diff --git a/packages/react-client/src/ReactFlightClient.js b/packages/react-client/src/ReactFlightClient.js
index e14b6a7699951..bbf513f996809 100644
--- a/packages/react-client/src/ReactFlightClient.js
+++ b/packages/react-client/src/ReactFlightClient.js
@@ -23,6 +23,7 @@ import {
   preloadModule,
   requireModule,
   parseModel,
+  dispatchDirective,
 } from './ReactFlightClientConfig';
 
 import {knownServerReferences} from './ReactFlightServerReferenceRegistry';
@@ -758,6 +759,15 @@ export function resolveErrorDev(
   }
 }
 
+export function resolveDirective(
+  response: Response,
+  id: number,
+  model: string,
+): void {
+  const payload = JSON.parse(model);
+  dispatchDirective(payload);
+}
+
 export function close(response: Response): void {
   // In case there are any remaining unresolved chunks, they won't
   // be resolved now. So we need to issue an error to those.
diff --git a/packages/react-client/src/ReactFlightClientStream.js b/packages/react-client/src/ReactFlightClientStream.js
index 81633e696696d..256424e6ae983 100644
--- a/packages/react-client/src/ReactFlightClientStream.js
+++ b/packages/react-client/src/ReactFlightClientStream.js
@@ -16,6 +16,7 @@ import {
   resolveModel,
   resolveErrorProd,
   resolveErrorDev,
+  resolveDirective,
   createResponse as createResponseBase,
   parseModelString,
   parseModelTuple,
@@ -46,6 +47,10 @@ function processFullRow(response: Response, row: string): void {
       resolveModule(response, id, row.substring(colon + 2));
       return;
     }
+    case 'D': {
+      resolveDirective(response, id, row.substring(colon + 2));
+      return;
+    }
     case 'E': {
       const errorInfo = JSON.parse(row.substring(colon + 2));
       if (__DEV__) {
diff --git a/packages/react-client/src/forks/ReactFlightClientConfig.custom.js b/packages/react-client/src/forks/ReactFlightClientConfig.custom.js
index 4990e84e7cb09..f4a4b9d4c0187 100644
--- a/packages/react-client/src/forks/ReactFlightClientConfig.custom.js
+++ b/packages/react-client/src/forks/ReactFlightClientConfig.custom.js
@@ -35,6 +35,7 @@ export const resolveClientReference = $$$config.resolveClientReference;
 export const resolveServerReference = $$$config.resolveServerReference;
 export const preloadModule = $$$config.preloadModule;
 export const requireModule = $$$config.requireModule;
+export const dispatchDirective = $$$config.dispatchDirective;
 
 export opaque type Source = mixed;
 
diff --git a/packages/react-dom-bindings/src/client/ReactFiberConfigDOM.js b/packages/react-dom-bindings/src/client/ReactFiberConfigDOM.js
index 705b057c80b32..85c0a1531980a 100644
--- a/packages/react-dom-bindings/src/client/ReactFiberConfigDOM.js
+++ b/packages/react-dom-bindings/src/client/ReactFiberConfigDOM.js
@@ -7,6 +7,7 @@
  * @flow
  */
 
+import type {HostDispatcher} from 'react-dom/src/ReactDOMDispatcher';
 import type {EventPriority} from 'react-reconciler/src/ReactEventPriorities';
 import type {DOMEventName} from '../events/DOMEventNames';
 import type {Fiber, FiberRoot} from 'react-reconciler/src/ReactInternalTypes';
@@ -1865,10 +1866,6 @@ export function clearSingleton(instance: Instance): void {
 
 export const supportsResources = true;
 
-// The resource types we support. currently they match the form for the as argument.
-// In the future this may need to change, especially when modules / scripts are supported
-type ResourceType = 'style' | 'font' | 'script';
-
 type HoistableTagType = 'link' | 'meta' | 'title';
 type TResource<
   T: 'stylesheet' | 'style' | 'script' | 'void',
@@ -1959,7 +1956,7 @@ function getDocumentFromRoot(root: HoistableRoot): Document {
 // We want this to be the default dispatcher on ReactDOMSharedInternals but we don't want to mutate
 // internals in Module scope. Instead we export it and Internals will import it. There is already a cycle
 // from Internals -> ReactDOM -> HostConfig -> Internals so this doesn't introduce a new one.
-export const ReactDOMClientDispatcher = {
+export const ReactDOMClientDispatcher: HostDispatcher = {
   prefetchDNS,
   preconnect,
   preload,
@@ -2033,7 +2030,10 @@ function prefetchDNS(href: string, options?: mixed) {
   preconnectAs('dns-prefetch', null, href);
 }
 
-function preconnect(href: string, options?: {crossOrigin?: string}) {
+function preconnect(href: string, options: ?{crossOrigin?: string}) {
+  if (!enableFloat) {
+    return;
+  }
   if (__DEV__) {
     if (typeof href !== 'string' || !href) {
       console.error(
@@ -2061,9 +2061,8 @@ function preconnect(href: string, options?: {crossOrigin?: string}) {
   preconnectAs('preconnect', crossOrigin, href);
 }
 
-type PreloadAs = ResourceType;
 type PreloadOptions = {
-  as: PreloadAs,
+  as: string,
   crossOrigin?: string,
   integrity?: string,
   type?: string,
@@ -2112,7 +2111,7 @@ function preload(href: string, options: PreloadOptions) {
 
 function preloadPropsFromPreloadOptions(
   href: string,
-  as: ResourceType,
+  as: string,
   options: PreloadOptions,
 ): PreloadProps {
   return {
@@ -2125,9 +2124,8 @@ function preloadPropsFromPreloadOptions(
   };
 }
 
-type PreinitAs = 'style' | 'script';
 type PreinitOptions = {
-  as: PreinitAs,
+  as: string,
   precedence?: string,
   crossOrigin?: string,
   integrity?: string,
diff --git a/packages/react-dom-bindings/src/server/ReactDOMLegacyServerStreamConfig.js b/packages/react-dom-bindings/src/server/ReactDOMLegacyServerStreamConfig.js
index f5a5356312fbe..c07bd229e43ce 100644
--- a/packages/react-dom-bindings/src/server/ReactDOMLegacyServerStreamConfig.js
+++ b/packages/react-dom-bindings/src/server/ReactDOMLegacyServerStreamConfig.js
@@ -23,6 +23,7 @@ export function flushBuffered(destination: Destination) {}
 
 export const supportsRequestStorage = false;
 export const requestStorage: AsyncLocalStorage<any> = (null: any);
+export const requestStorage2: AsyncLocalStorage<any> = (null: any);
 
 export function beginWriting(destination: Destination) {}
 
diff --git a/packages/react-dom-bindings/src/server/ReactFizzConfigDOM.js b/packages/react-dom-bindings/src/server/ReactFizzConfigDOM.js
index 9f1aba93a9a21..fad0162a601a9 100644
--- a/packages/react-dom-bindings/src/server/ReactFizzConfigDOM.js
+++ b/packages/react-dom-bindings/src/server/ReactFizzConfigDOM.js
@@ -37,6 +37,11 @@ import {
   stringToPrecomputedChunk,
   clonePrecomputedChunk,
 } from 'react-server/src/ReactServerStreamConfig';
+import {
+  resolveResources,
+  setCurrentResources,
+  getCurrentResources,
+} from 'react-server/src/ReactFizzResources';
 
 import isAttributeNameSafe from '../shared/isAttributeNameSafe';
 import isUnitlessNumber from '../shared/isUnitlessNumber';
@@ -78,30 +83,34 @@ import {
 import ReactDOMSharedInternals from 'shared/ReactDOMSharedInternals';
 const ReactDOMCurrentDispatcher = ReactDOMSharedInternals.Dispatcher;
 
-const ReactDOMServerDispatcher = enableFloat
-  ? {
-      prefetchDNS,
-      preconnect,
-      preload,
-      preinit,
-    }
-  : {};
+const ReactDOMServerDispatcher = {
+  prefetchDNS,
+  preconnect,
+  preload,
+  preinit,
+};
 
-let currentResources: null | Resources = null;
 const currentResourcesStack = [];
 
-export function prepareToRender(resources: Resources): mixed {
-  currentResourcesStack.push(currentResources);
-  currentResources = resources;
+function pushResources(resources: null | Resources) {
+  currentResourcesStack.push(getCurrentResources());
+  setCurrentResources(resources);
+}
 
-  const previousHostDispatcher = ReactDOMCurrentDispatcher.current;
+function popResources() {
+  setCurrentResources(currentResourcesStack.pop());
+}
+
+export function prepareHostDispatcher() {
   ReactDOMCurrentDispatcher.current = ReactDOMServerDispatcher;
-  return previousHostDispatcher;
 }
 
-export function cleanupAfterRender(previousDispatcher: mixed) {
-  currentResources = currentResourcesStack.pop();
-  ReactDOMCurrentDispatcher.current = previousDispatcher;
+export function prepareToRender(resources: Resources): mixed {
+  pushResources(resources);
+}
+
+export function cleanupAfterRender() {
+  popResources();
 }
 
 // Used to distinguish these contexts from ones used in other renderers.
@@ -4490,16 +4499,18 @@ function getResourceKey(as: string, href: string): string {
 }
 
 export function prefetchDNS(href: string, options?: mixed) {
-  if (!currentResources) {
-    // While we expect that preconnect calls are primarily going to be observed
-    // during render because effects and events don't run on the server it is
-    // still possible that these get called in module scope. This is valid on
-    // the client since there is still a document to interact with but on the
-    // server we need a request to associate the call to. Because of this we
-    // simply return and do not warn.
+  if (!enableFloat) {
+    return;
+  }
+  const resources = resolveResources();
+  if (!resources) {
+    // In async contexts we can sometimes resolve resources from AsyncLocalStorage. If we can't we can also
+    // possibly get them from the stack if we are not in an async context. Since we were not able to resolve
+    // the resources for this call in either case we opt to do nothing. We can consider making this a warning
+    // but there may be times where calling a function outside of render is intentional (i.e. to warm up data
+    // fetching) and we don't want to warn in those cases.
     return;
   }
-  const resources = currentResources;
   if (__DEV__) {
     if (typeof href !== 'string' || !href) {
       console.error(
@@ -4544,17 +4555,19 @@ export function prefetchDNS(href: string, options?: mixed) {
   }
 }
 
-export function preconnect(href: string, options?: {crossOrigin?: string}) {
-  if (!currentResources) {
-    // While we expect that preconnect calls are primarily going to be observed
-    // during render because effects and events don't run on the server it is
-    // still possible that these get called in module scope. This is valid on
-    // the client since there is still a document to interact with but on the
-    // server we need a request to associate the call to. Because of this we
-    // simply return and do not warn.
+export function preconnect(href: string, options?: ?{crossOrigin?: string}) {
+  if (!enableFloat) {
+    return;
+  }
+  const resources = resolveResources();
+  if (!resources) {
+    // In async contexts we can sometimes resolve resources from AsyncLocalStorage. If we can't we can also
+    // possibly get them from the stack if we are not in an async context. Since we were not able to resolve
+    // the resources for this call in either case we opt to do nothing. We can consider making this a warning
+    // but there may be times where calling a function outside of render is intentional (i.e. to warm up data
+    // fetching) and we don't want to warn in those cases.
     return;
   }
-  const resources = currentResources;
   if (__DEV__) {
     if (typeof href !== 'string' || !href) {
       console.error(
@@ -4603,24 +4616,25 @@ export function preconnect(href: string, options?: {crossOrigin?: string}) {
   }
 }
 
-type PreloadAs = 'style' | 'font' | 'script';
 type PreloadOptions = {
-  as: PreloadAs,
+  as: string,
   crossOrigin?: string,
   integrity?: string,
   type?: string,
 };
 export function preload(href: string, options: PreloadOptions) {
-  if (!currentResources) {
-    // While we expect that preload calls are primarily going to be observed
-    // during render because effects and events don't run on the server it is
-    // still possible that these get called in module scope. This is valid on
-    // the client since there is still a document to interact with but on the
-    // server we need a request to associate the call to. Because of this we
-    // simply return and do not warn.
+  if (!enableFloat) {
+    return;
+  }
+  const resources = resolveResources();
+  if (!resources) {
+    // In async contexts we can sometimes resolve resources from AsyncLocalStorage. If we can't we can also
+    // possibly get them from the stack if we are not in an async context. Since we were not able to resolve
+    // the resources for this call in either case we opt to do nothing. We can consider making this a warning
+    // but there may be times where calling a function outside of render is intentional (i.e. to warm up data
+    // fetching) and we don't want to warn in those cases.
     return;
   }
-  const resources = currentResources;
   if (__DEV__) {
     if (typeof href !== 'string' || !href) {
       console.error(
@@ -4744,24 +4758,26 @@ export function preload(href: string, options: PreloadOptions) {
   }
 }
 
-type PreinitAs = 'style' | 'script';
 type PreinitOptions = {
-  as: PreinitAs,
+  as: string,
   precedence?: string,
   crossOrigin?: string,
   integrity?: string,
 };
 export function preinit(href: string, options: PreinitOptions): void {
-  if (!currentResources) {
-    // While we expect that preinit calls are primarily going to be observed
-    // during render because effects and events don't run on the server it is
-    // still possible that these get called in module scope. This is valid on
-    // the client since there is still a document to interact with but on the
-    // server we need a request to associate the call to. Because of this we
-    // simply return and do not warn.
+  if (!enableFloat) {
     return;
   }
-  preinitImpl(currentResources, href, options);
+  const resources = resolveResources();
+  if (!resources) {
+    // In async contexts we can sometimes resolve resources from AsyncLocalStorage. If we can't we can also
+    // possibly get them from the stack if we are not in an async context. Since we were not able to resolve
+    // the resources for this call in either case we opt to do nothing. We can consider making this a warning
+    // but there may be times where calling a function outside of render is intentional (i.e. to warm up data
+    // fetching) and we don't want to warn in those cases.
+    return;
+  }
+  preinitImpl(resources, href, options);
 }
 
 // On the server, preinit may be called outside of render when sending an
@@ -4983,7 +4999,7 @@ function preinitImpl(
 
 function preloadPropsFromPreloadOptions(
   href: string,
-  as: PreloadAs,
+  as: string,
   options: PreloadOptions,
 ): PreloadProps {
   return {
diff --git a/packages/react-dom-bindings/src/server/ReactFizzConfigDOMLegacy.js b/packages/react-dom-bindings/src/server/ReactFizzConfigDOMLegacy.js
index 1707b4d2c13e3..f7cc6500739d8 100644
--- a/packages/react-dom-bindings/src/server/ReactFizzConfigDOMLegacy.js
+++ b/packages/react-dom-bindings/src/server/ReactFizzConfigDOMLegacy.js
@@ -137,6 +137,7 @@ export {
   writePostamble,
   hoistResources,
   setCurrentlyRenderingBoundaryResourcesTarget,
+  prepareHostDispatcher,
   prepareToRender,
   cleanupAfterRender,
 } from './ReactFizzConfigDOM';
diff --git a/packages/react-dom-bindings/src/server/ReactFlightServerConfigDOM.js b/packages/react-dom-bindings/src/server/ReactFlightServerConfigDOM.js
index e2daf606c8ebd..5be33bfd2c18b 100644
--- a/packages/react-dom-bindings/src/server/ReactFlightServerConfigDOM.js
+++ b/packages/react-dom-bindings/src/server/ReactFlightServerConfigDOM.js
@@ -7,6 +7,96 @@
  * @flow
  */
 
+import {enableFloat} from 'shared/ReactFeatureFlags';
+
+import {resolveDirectives} from 'react-server/src/ReactFlightDirectives';
+
+import ReactDOMSharedInternals from 'shared/ReactDOMSharedInternals';
+const ReactDOMCurrentDispatcher = ReactDOMSharedInternals.Dispatcher;
+
+const ReactDOMFlightServerDispatcher = {
+  prefetchDNS,
+  preconnect,
+  preload,
+  preinit,
+};
+
+export function prepareHostDispatcher(): void {
+  ReactDOMCurrentDispatcher.current = ReactDOMFlightServerDispatcher;
+}
+
 // Used to distinguish these contexts from ones used in other renderers.
 // E.g. this can be used to distinguish legacy renderers from this modern one.
 export const isPrimaryRenderer = true;
+
+let didWarnAsyncEnvironmentDev = false;
+
+type TDirective<Method, Options> = {
+  method: Method,
+  href: string,
+  options: Options,
+};
+export type Directive =
+  | PrefetchDNSDirective
+  | PreconnectDirective
+  | PreloadDirective
+  | PreinitDirective;
+type PrefetchDNSDirective = TDirective<'prefetchDNS', void>;
+type PreconnectDirective = TDirective<'preconnect', ?{crossOrigin?: string}>;
+type PreloadDirective = TDirective<'preload', PreloadOptions>;
+type PreinitDirective = TDirective<'preinit', PreinitOptions>;
+
+export function prefetchDNS(href: string, options?: mixed) {
+  if (enableFloat) {
+    pushDirective({method: 'prefetchDNS', href, options: (options: any)});
+  }
+}
+
+export function preconnect(href: string, options: ?{crossOrigin?: string}) {
+  if (enableFloat) {
+    pushDirective({method: 'preconnect', href, options});
+  }
+}
+
+type PreloadOptions = {
+  as: string,
+  crossOrigin?: string,
+  integrity?: string,
+  type?: string,
+};
+
+export function preload(href: string, options: PreloadOptions) {
+  if (enableFloat) {
+    pushDirective({method: 'preload', href, options});
+  }
+}
+
+type PreinitOptions = {
+  as: string,
+  precedence?: string,
+  crossOrigin?: string,
+  integrity?: string,
+};
+export function preinit(href: string, options: PreinitOptions): void {
+  if (enableFloat) {
+    pushDirective({method: 'preinit', href, options});
+  }
+}
+
+function pushDirective(directive: Directive): void {
+  const directives = resolveDirectives();
+  if (directives === null) {
+    if (__DEV__) {
+      if (!didWarnAsyncEnvironmentDev) {
+        didWarnAsyncEnvironmentDev = true;
+        console.error(
+          'ReactDOM.%s(): React expected to be able to associate this call to a specific Request but cannot. It is possible that this call was invoked outside of a React component. If you are calling it from within a React component that is an async function after the first `await` then you are in an environment which does not support AsyncLocalStorage. In this kind of environment ReactDOM.%s() does not do anything when called in an async manner. Try moving this function call above the first `await` within the component or remove this call. In environments that support AsyncLocalStorage such as Node.js you can call this method anywhere in a React component even after `await` operator.',
+          directive.method,
+          directive.method,
+        );
+      }
+    }
+    return;
+  }
+  directives.push(directive);
+}
diff --git a/packages/react-dom-bindings/src/shared/ReactFlightClientConfigDOM.js b/packages/react-dom-bindings/src/shared/ReactFlightClientConfigDOM.js
index d92d7d50ea060..0125ca260badb 100644
--- a/packages/react-dom-bindings/src/shared/ReactFlightClientConfigDOM.js
+++ b/packages/react-dom-bindings/src/shared/ReactFlightClientConfigDOM.js
@@ -10,4 +10,27 @@
 // This client file is in the shared folder because it applies to both SSR and browser contexts.
 // It is the configuraiton of the FlightClient behavior which can run in either environment.
 
-// In a future update this is where we will implement `dispatchDirective` such as for Float methods
+import type {Directive} from '../server/ReactFlightServerConfigDOM';
+
+import ReactDOMSharedInternals from 'shared/ReactDOMSharedInternals';
+const ReactDOMCurrentDispatcher = ReactDOMSharedInternals.Dispatcher;
+
+export function dispatchDirective(directive: Directive): void {
+  const dispatcher = ReactDOMCurrentDispatcher.current;
+  if (dispatcher) {
+    switch (directive.method) {
+      case 'prefetchDNS':
+        dispatcher.prefetchDNS(directive.href, directive.options);
+        return;
+      case 'preconnect':
+        dispatcher.preconnect(directive.href, directive.options);
+        return;
+      case 'preload':
+        dispatcher.preload(directive.href, directive.options);
+        return;
+      case 'preinit':
+        dispatcher.preinit(directive.href, directive.options);
+        return;
+    }
+  }
+}
diff --git a/packages/react-dom/src/ReactDOMDispatcher.js b/packages/react-dom/src/ReactDOMDispatcher.js
new file mode 100644
index 0000000000000..f5fecc913ea4f
--- /dev/null
+++ b/packages/react-dom/src/ReactDOMDispatcher.js
@@ -0,0 +1,30 @@
+/**
+ * Copyright (c) Meta Platforms, Inc. and affiliates.
+ *
+ * This source code is licensed under the MIT license found in the
+ * LICENSE file in the root directory of this source tree.
+ *
+ * @flow
+ */
+
+export type PrefetchDNSOptions = void;
+export type PreconnectOptions = {crossOrigin?: string};
+export type PreloadOptions = {
+  as: string,
+  crossOrigin?: string,
+  integrity?: string,
+  type?: string,
+};
+export type PreinitOptions = {
+  as: string,
+  precedence?: string,
+  crossOrigin?: string,
+  integrity?: string,
+};
+
+export type HostDispatcher = {
+  prefetchDNS: (href: string, options?: ?PrefetchDNSOptions) => void,
+  preconnect: (href: string, options: ?PreconnectOptions) => void,
+  preload: (href: string, options: PreloadOptions) => void,
+  preinit: (href: string, options: PreinitOptions) => void,
+};
diff --git a/packages/react-dom/src/ReactDOMFloat.js b/packages/react-dom/src/ReactDOMFloat.js
index 99a867286d361..25a03fcd092e9 100644
--- a/packages/react-dom/src/ReactDOMFloat.js
+++ b/packages/react-dom/src/ReactDOMFloat.js
@@ -1,39 +1,72 @@
+/**
+ * Copyright (c) Meta Platforms, Inc. and affiliates.
+ *
+ * This source code is licensed under the MIT license found in the
+ * LICENSE file in the root directory of this source tree.
+ *
+ * @flow
+ */
+import type {
+  PreconnectOptions,
+  PreloadOptions,
+  PreinitOptions,
+} from './ReactDOMDispatcher';
+
 import ReactDOMSharedInternals from 'shared/ReactDOMSharedInternals';
+const Dispatcher = ReactDOMSharedInternals.Dispatcher;
 
-export function prefetchDNS() {
-  const dispatcher = ReactDOMSharedInternals.Dispatcher.current;
+export function prefetchDNS(href: string) {
+  let passedOptionArg: any;
+  if (__DEV__) {
+    if (arguments[1] !== undefined) {
+      passedOptionArg = arguments[1];
+    }
+  }
+  const dispatcher = Dispatcher.current;
   if (dispatcher) {
-    dispatcher.prefetchDNS.apply(this, arguments);
+    if (__DEV__) {
+      if (passedOptionArg !== undefined) {
+        // prefetchDNS will warn if you pass reserved options arg. We pass it along in Dev only to
+        // elicit the warning. In prod we do not forward since it is not a part of the interface.
+        // @TODO move all arg validation into this file. It needs to be universal anyway so may as well lock down the interace here and
+        // let the rest of the codebase trust the types
+        dispatcher.prefetchDNS(href, passedOptionArg);
+      } else {
+        dispatcher.prefetchDNS(href);
+      }
+    } else {
+      dispatcher.prefetchDNS(href);
+    }
   }
   // We don't error because preconnect needs to be resilient to being called in a variety of scopes
   // and the runtime may not be capable of responding. The function is optimistic and not critical
   // so we favor silent bailout over warning or erroring.
 }
 
-export function preconnect() {
-  const dispatcher = ReactDOMSharedInternals.Dispatcher.current;
+export function preconnect(href: string, options?: ?PreconnectOptions) {
+  const dispatcher = Dispatcher.current;
   if (dispatcher) {
-    dispatcher.preconnect.apply(this, arguments);
+    dispatcher.preconnect(href, options);
   }
   // We don't error because preconnect needs to be resilient to being called in a variety of scopes
   // and the runtime may not be capable of responding. The function is optimistic and not critical
   // so we favor silent bailout over warning or erroring.
 }
 
-export function preload() {
-  const dispatcher = ReactDOMSharedInternals.Dispatcher.current;
+export function preload(href: string, options: PreloadOptions) {
+  const dispatcher = Dispatcher.current;
   if (dispatcher) {
-    dispatcher.preload.apply(this, arguments);
+    dispatcher.preload(href, options);
   }
   // We don't error because preload needs to be resilient to being called in a variety of scopes
   // and the runtime may not be capable of responding. The function is optimistic and not critical
   // so we favor silent bailout over warning or erroring.
 }
 
-export function preinit() {
-  const dispatcher = ReactDOMSharedInternals.Dispatcher.current;
+export function preinit(href: string, options: PreinitOptions) {
+  const dispatcher = Dispatcher.current;
   if (dispatcher) {
-    dispatcher.preinit.apply(this, arguments);
+    dispatcher.preinit(href, options);
   }
   // We don't error because preinit needs to be resilient to being called in a variety of scopes
   // and the runtime may not be capable of responding. The function is optimistic and not critical
diff --git a/packages/react-dom/src/ReactDOMSharedInternals.js b/packages/react-dom/src/ReactDOMSharedInternals.js
index a9e0407b006b2..cf2909ffac2ff 100644
--- a/packages/react-dom/src/ReactDOMSharedInternals.js
+++ b/packages/react-dom/src/ReactDOMSharedInternals.js
@@ -7,11 +7,13 @@
  * @flow
  */
 
+import type {HostDispatcher} from './ReactDOMDispatcher';
+
 type InternalsType = {
   usingClientEntryPoint: boolean,
   Events: [any, any, any, any, any, any],
   Dispatcher: {
-    current: mixed,
+    current: null | HostDispatcher,
   },
 };
 
diff --git a/packages/react-dom/src/__tests__/ReactDOMFloat-test.js b/packages/react-dom/src/__tests__/ReactDOMFloat-test.js
index 8617f9be56179..c0ea39665fcff 100644
--- a/packages/react-dom/src/__tests__/ReactDOMFloat-test.js
+++ b/packages/react-dom/src/__tests__/ReactDOMFloat-test.js
@@ -3979,7 +3979,7 @@ body {
     });
 
     // @gate enableFloat
-    it('creates a preload resource when ReactDOM.preinit(..., {as: "script" }) is called outside of render on the client', async () => {
+    it('creates a script resource when ReactDOM.preinit(..., {as: "script" }) is called outside of render on the client', async () => {
       function App() {
         React.useEffect(() => {
           ReactDOM.preinit('foo', {as: 'script'});
diff --git a/packages/react-dom/src/client/ReactDOMRoot.js b/packages/react-dom/src/client/ReactDOMRoot.js
index e79fa16452bda..1ec50536586dd 100644
--- a/packages/react-dom/src/client/ReactDOMRoot.js
+++ b/packages/react-dom/src/client/ReactDOMRoot.js
@@ -13,8 +13,6 @@ import type {
   TransitionTracingCallbacks,
 } from 'react-reconciler/src/ReactInternalTypes';
 
-import ReactDOMSharedInternals from '../ReactDOMSharedInternals';
-const {Dispatcher} = ReactDOMSharedInternals;
 import {ReactDOMClientDispatcher} from 'react-dom-bindings/src/client/ReactFiberConfigDOM';
 import {queueExplicitHydrationTarget} from 'react-dom-bindings/src/events/ReactDOMEventReplaying';
 import {REACT_ELEMENT_TYPE} from 'shared/ReactSymbols';
@@ -25,13 +23,19 @@ import {
   disableCommentsAsDOMContainers,
 } from 'shared/ReactFeatureFlags';
 
+import ReactDOMSharedInternals from '../ReactDOMSharedInternals';
+const {Dispatcher} = ReactDOMSharedInternals;
+if (enableFloat) {
+  // Set the default dispatcher to the client dispatcher
+  Dispatcher.current = ReactDOMClientDispatcher;
+}
+
 export type RootType = {
   render(children: ReactNodeList): void,
   unmount(): void,
   _internalRoot: FiberRoot | null,
   ...
 };
-
 export type CreateRootOptions = {
   unstable_strictMode?: boolean,
   unstable_concurrentUpdatesByDefault?: boolean,
diff --git a/packages/react-native-renderer/src/server/ReactFizzConfigNative.js b/packages/react-native-renderer/src/server/ReactFizzConfigNative.js
index 54650e851f614..c1c3ac8e517f5 100644
--- a/packages/react-native-renderer/src/server/ReactFizzConfigNative.js
+++ b/packages/react-native-renderer/src/server/ReactFizzConfigNative.js
@@ -339,6 +339,7 @@ export function hoistResources(
   boundaryResources: BoundaryResources,
 ) {}
 
+export function prepareHostDispatcher() {}
 export function prepareToRender(resources: Resources) {}
 export function cleanupAfterRender(previousDispatcher: mixed) {}
 export function createResources() {}
diff --git a/packages/react-native-renderer/src/server/ReactFlightServerConfigNative.js b/packages/react-native-renderer/src/server/ReactFlightServerConfigNative.js
index cc92e90d8b342..7a8dc23d39cc2 100644
--- a/packages/react-native-renderer/src/server/ReactFlightServerConfigNative.js
+++ b/packages/react-native-renderer/src/server/ReactFlightServerConfigNative.js
@@ -8,3 +8,7 @@
  */
 
 export const isPrimaryRenderer = true;
+
+export type Directive = void;
+
+export function prepareHostDispatcher() {}
diff --git a/packages/react-noop-renderer/src/ReactNoopFlightServer.js b/packages/react-noop-renderer/src/ReactNoopFlightServer.js
index 52794a6221c3f..32b3aa2c4f21e 100644
--- a/packages/react-noop-renderer/src/ReactNoopFlightServer.js
+++ b/packages/react-noop-renderer/src/ReactNoopFlightServer.js
@@ -63,6 +63,7 @@ const ReactNoopFlightServer = ReactFlightServer({
   ) {
     return saveModule(reference.value);
   },
+  prepareHostDispatcher() {},
 });
 
 type Options = {
diff --git a/packages/react-noop-renderer/src/ReactNoopServer.js b/packages/react-noop-renderer/src/ReactNoopServer.js
index cd5edd94d29d6..cb125e0c112ce 100644
--- a/packages/react-noop-renderer/src/ReactNoopServer.js
+++ b/packages/react-noop-renderer/src/ReactNoopServer.js
@@ -279,6 +279,7 @@ const ReactNoopServer = ReactFizzServer({
 
   setCurrentlyRenderingBoundaryResourcesTarget(resources: BoundaryResources) {},
 
+  prepareHostDispatcher() {},
   prepareToRender() {},
   cleanupAfterRender() {},
 });
diff --git a/packages/react-server-dom-relay/src/ReactFlightDOMRelayProtocol.js b/packages/react-server-dom-relay/src/ReactFlightDOMRelayProtocol.js
index 73b793f0d715c..b16d860b00968 100644
--- a/packages/react-server-dom-relay/src/ReactFlightDOMRelayProtocol.js
+++ b/packages/react-server-dom-relay/src/ReactFlightDOMRelayProtocol.js
@@ -20,6 +20,7 @@ export type JSONValue =
 export type RowEncoding =
   | ['O', number, JSONValue]
   | ['I', number, ClientReferenceMetadata]
+  | ['D', number, JSONValue]
   | ['P', number, string]
   | ['S', number, string]
   | [
diff --git a/packages/react-server-dom-relay/src/ReactFlightServerConfigDOMRelay.js b/packages/react-server-dom-relay/src/ReactFlightServerConfigDOMRelay.js
index 0f709b7dbcc24..869a46e04092a 100644
--- a/packages/react-server-dom-relay/src/ReactFlightServerConfigDOMRelay.js
+++ b/packages/react-server-dom-relay/src/ReactFlightServerConfigDOMRelay.js
@@ -7,6 +7,8 @@
  * @flow
  */
 
+import type {Directive} from 'react-dom-bindings/src/server/ReactFlightServerConfigDOM';
+import type {Resources} from 'react-server/src/ReactFizzConfig';
 import type {RowEncoding, JSONValue} from './ReactFlightDOMRelayProtocol';
 
 import type {
@@ -191,6 +193,16 @@ export function processImportChunk(
   return ['I', id, clientReferenceMetadata];
 }
 
+export function processDirectiveChunk(
+  request: Request,
+  id: number,
+  payload: ReactClientValue,
+): Chunk {
+  // The clientReferenceMetadata is already a JSON serializable value.
+  const json = convertModelToJSON(request, {}, '', payload);
+  return ['D', id, json];
+}
+
 export function scheduleWork(callback: () => void) {
   callback();
 }
@@ -198,8 +210,11 @@ export function scheduleWork(callback: () => void) {
 export function flushBuffered(destination: Destination) {}
 
 export const supportsRequestStorage = false;
-export const requestStorage: AsyncLocalStorage<Map<Function, mixed>> =
-  (null: any);
+export const requestStorage: AsyncLocalStorage<{
+  cache: Map<Function, mixed>,
+  directives: Array<Directive>,
+}> = (null: any);
+export const requestStorage2: AsyncLocalStorage<Resources> = (null: any);
 
 export function beginWriting(destination: Destination) {}
 
diff --git a/packages/react-server-dom-relay/src/ReactServerStreamConfigFB.js b/packages/react-server-dom-relay/src/ReactServerStreamConfigFB.js
index bc550d63ea7ea..87245e956d463 100644
--- a/packages/react-server-dom-relay/src/ReactServerStreamConfigFB.js
+++ b/packages/react-server-dom-relay/src/ReactServerStreamConfigFB.js
@@ -7,6 +7,8 @@
  * @flow
  */
 
+import type {Resources} from 'react-server/src/ReactFizzConfig';
+
 export type Destination = {
   buffer: string,
   done: boolean,
@@ -24,8 +26,11 @@ export function scheduleWork(callback: () => void) {
 export function flushBuffered(destination: Destination) {}
 
 export const supportsRequestStorage = false;
-export const requestStorage: AsyncLocalStorage<Map<Function, mixed>> =
-  (null: any);
+export const requestStorage: AsyncLocalStorage<{
+  cache: Map<Function, mixed>,
+  directives: Array<string>,
+}> = (null: any);
+export const requestStorage2: AsyncLocalStorage<Resources> = (null: any);
 
 export function beginWriting(destination: Destination) {}
 
diff --git a/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOM-test.js b/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOM-test.js
index b2a25dec436da..abf723955d0e9 100644
--- a/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOM-test.js
+++ b/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOM-test.js
@@ -25,9 +25,11 @@ let clientModuleError;
 let webpackMap;
 let Stream;
 let React;
+let ReactDOM;
 let ReactDOMClient;
 let ReactServerDOMServer;
 let ReactServerDOMClient;
+let ReactDOMFizzServer;
 let Suspense;
 let ErrorBoundary;
 
@@ -42,6 +44,8 @@ describe('ReactFlightDOM', () => {
 
     Stream = require('stream');
     React = require('react');
+    ReactDOM = require('react-dom');
+    ReactDOMFizzServer = require('react-dom/server.node');
     use = React.use;
     Suspense = React.Suspense;
     ReactDOMClient = require('react-dom/client');
@@ -1114,4 +1118,229 @@ describe('ReactFlightDOM', () => {
     );
     expect(reportedErrors).toEqual([theError]);
   });
+
+  // @gate enableUseHook
+  it('should support ReactDOM.preload when rendering in Fiber', async () => {
+    function Component() {
+      return <p>hello world</p>;
+    }
+
+    const ClientComponent = clientExports(Component);
+
+    async function ServerComponent() {
+      ReactDOM.preload('before', {as: 'style'});
+      await 1;
+      ReactDOM.preload('after', {as: 'style'});
+      return <ClientComponent />;
+    }
+
+    const {writable, readable} = getTestStream();
+    const {pipe} = ReactServerDOMServer.renderToPipeableStream(
+      <ServerComponent />,
+      webpackMap,
+    );
+    pipe(writable);
+
+    let response = null;
+    function getResponse() {
+      if (response === null) {
+        response = ReactServerDOMClient.createFromReadableStream(readable);
+      }
+      return response;
+    }
+
+    function App() {
+      return getResponse();
+    }
+
+    // We pause to allow the float call after the await point to process before the
+    // HostDispatcher gets set for Fiber by createRoot. This is only needed in testing
+    // because the module graphs are not different and the HostDispatcher is shared.
+    // In a real environment the Fiber and Flight code would each have their own independent
+    // dispatcher.
+    // @TODO consider what happens when Server-Components-On-The-Client exist. we probably
+    // want to use the Fiber HostDispatcher there too since it is more about the host than the runtime
+    // but we need to make sure that actually makes sense
+    await 1;
+
+    const container = document.createElement('div');
+    const root = ReactDOMClient.createRoot(container);
+    await act(() => {
+      root.render(<App />);
+    });
+    expect(document.head.innerHTML).toBe(
+      '<link href="before" rel="preload" as="style">' +
+        '<link href="after" rel="preload" as="style">',
+    );
+    expect(container.innerHTML).toBe('<p>hello world</p>');
+  });
+
+  // @gate enableUseHook
+  it('should support ReactDOM.preload when rendering in Fizz', async () => {
+    function Component() {
+      return <p>hello world</p>;
+    }
+
+    const ClientComponent = clientExports(Component);
+
+    async function ServerComponent() {
+      ReactDOM.preload('before', {as: 'style'});
+      await 1;
+      ReactDOM.preload('after', {as: 'style'});
+      return <ClientComponent />;
+    }
+
+    const {writable: flightWritable, readable: flightReadable} =
+      getTestStream();
+    const {writable: fizzWritable, readable: fizzReadable} = getTestStream();
+
+    // In a real environment you would want to call the render during the Fizz render.
+    // The reason we cannot do this in our test is because we don't actually have two separate
+    // module graphs and we are contriving the sequencing to work in a way where
+    // the right HostDispatcher is in scope during the Flight Server Float calls and the
+    // Flight Client directive dispatches
+    const {pipe} = ReactServerDOMServer.renderToPipeableStream(
+      <ServerComponent />,
+      webpackMap,
+    );
+    pipe(flightWritable);
+
+    let response = null;
+    function getResponse() {
+      if (response === null) {
+        response =
+          ReactServerDOMClient.createFromReadableStream(flightReadable);
+      }
+      return response;
+    }
+
+    function App() {
+      return (
+        <html>
+          <body>{getResponse()}</body>
+        </html>
+      );
+    }
+
+    await act(async () => {
+      ReactDOMFizzServer.renderToPipeableStream(<App />).pipe(fizzWritable);
+    });
+
+    const decoder = new TextDecoder();
+    const reader = fizzReadable.getReader();
+    let content = '';
+    while (true) {
+      const {done, value} = await reader.read();
+      if (done) {
+        content += decoder.decode();
+        break;
+      }
+      content += decoder.decode(value, {stream: true});
+    }
+
+    expect(content).toEqual(
+      '<!DOCTYPE html><html><head><link rel="preload" as="style" href="before"/>' +
+        '<link rel="preload" as="style" href="after"/></head><body><p>hello world</p></body></html>',
+    );
+  });
+
+  it('supports Float directives from concurrent Flight -> Fizz renders', async () => {
+    function Component() {
+      return <p>hello world</p>;
+    }
+
+    const ClientComponent = clientExports(Component);
+
+    async function ServerComponent1() {
+      ReactDOM.preload('before1', {as: 'style'});
+      await 1;
+      ReactDOM.preload('after1', {as: 'style'});
+      return <ClientComponent />;
+    }
+
+    async function ServerComponent2() {
+      ReactDOM.preload('before2', {as: 'style'});
+      await 1;
+      ReactDOM.preload('after2', {as: 'style'});
+      return <ClientComponent />;
+    }
+
+    const {writable: flightWritable1, readable: flightReadable1} =
+      getTestStream();
+    const {writable: flightWritable2, readable: flightReadable2} =
+      getTestStream();
+
+    ReactServerDOMServer.renderToPipeableStream(
+      <ServerComponent1 />,
+      webpackMap,
+    ).pipe(flightWritable1);
+
+    ReactServerDOMServer.renderToPipeableStream(
+      <ServerComponent2 />,
+      webpackMap,
+    ).pipe(flightWritable2);
+
+    const responses = new Map();
+    function getResponse(stream) {
+      let response = responses.get(stream);
+      if (!response) {
+        response = ReactServerDOMClient.createFromReadableStream(stream);
+        responses.set(stream, response);
+      }
+      return response;
+    }
+
+    function App({stream}) {
+      return (
+        <html>
+          <body>{getResponse(stream)}</body>
+        </html>
+      );
+    }
+
+    // pausing to let Flight runtime tick. This is a test only artifact of the fact that
+    // we aren't operating separate module graphs for flight and fiber. In a real app
+    // each would have their own dispatcher and there would be no cross dispatching.
+    await 1;
+
+    const {writable: fizzWritable1, readable: fizzReadable1} = getTestStream();
+    const {writable: fizzWritable2, readable: fizzReadable2} = getTestStream();
+    await act(async () => {
+      ReactDOMFizzServer.renderToPipeableStream(
+        <App stream={flightReadable1} />,
+      ).pipe(fizzWritable1);
+      ReactDOMFizzServer.renderToPipeableStream(
+        <App stream={flightReadable2} />,
+      ).pipe(fizzWritable2);
+    });
+
+    async function read(stream) {
+      const decoder = new TextDecoder();
+      const reader = stream.getReader();
+      let buffer = '';
+      while (true) {
+        const {done, value} = await reader.read();
+        if (done) {
+          buffer += decoder.decode();
+          break;
+        }
+        buffer += decoder.decode(value, {stream: true});
+      }
+      return buffer;
+    }
+
+    const [content1, content2] = await Promise.all([
+      read(fizzReadable1),
+      read(fizzReadable2),
+    ]);
+
+    expect(content1).toEqual(
+      '<!DOCTYPE html><html><head><link rel="preload" as="style" href="before1"/>' +
+        '<link rel="preload" as="style" href="after1"/></head><body><p>hello world</p></body></html>',
+    );
+    expect(content2).toEqual(
+      '<!DOCTYPE html><html><head><link rel="preload" as="style" href="before2"/>' +
+        '<link rel="preload" as="style" href="after2"/></head><body><p>hello world</p></body></html>',
+    );
+  });
 });
diff --git a/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMBrowser-test.js b/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMBrowser-test.js
index d53a9df2e3eb8..272d170208c1c 100644
--- a/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMBrowser-test.js
+++ b/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMBrowser-test.js
@@ -21,7 +21,9 @@ let webpackMap;
 let webpackServerMap;
 let act;
 let React;
+let ReactDOM;
 let ReactDOMClient;
+let ReactDOMFizzServer;
 let ReactServerDOMServer;
 let ReactServerDOMClient;
 let Suspense;
@@ -37,7 +39,9 @@ describe('ReactFlightDOMBrowser', () => {
     webpackMap = WebpackMock.webpackMap;
     webpackServerMap = WebpackMock.webpackServerMap;
     React = require('react');
+    ReactDOM = require('react-dom');
     ReactDOMClient = require('react-dom/client');
+    ReactDOMFizzServer = require('react-dom/server.browser');
     ReactServerDOMServer = require('react-server-dom-webpack/server.browser');
     ReactServerDOMClient = require('react-server-dom-webpack/client');
     Suspense = React.Suspense;
@@ -929,4 +933,128 @@ describe('ReactFlightDOMBrowser', () => {
       expect(thrownError.digest).toBe('test-error-digest');
     }
   });
+
+  it('supports Float directives before the first await in server components in Fiber', async () => {
+    function Component() {
+      return <p>hello world</p>;
+    }
+
+    const ClientComponent = clientExports(Component);
+
+    async function ServerComponent() {
+      ReactDOM.preload('before', {as: 'style'});
+      await 1;
+      ReactDOM.preload('after', {as: 'style'});
+      return <ClientComponent />;
+    }
+
+    const stream = ReactServerDOMServer.renderToReadableStream(
+      <ServerComponent />,
+      webpackMap,
+    );
+
+    let response = null;
+    function getResponse() {
+      if (response === null) {
+        response = ReactServerDOMClient.createFromReadableStream(stream);
+      }
+      return response;
+    }
+
+    function App() {
+      return getResponse();
+    }
+
+    // pausing to let Flight runtime tick. This is a test only artifact of the fact that
+    // we aren't operating separate module graphs for flight and fiber. In a real app
+    // each would have their own dispatcher and there would be no cross dispatching.
+    await expect(async () => {
+      await 1;
+    }).toErrorDev(
+      'ReactDOM.preload(): React expected to be able to associate this call to a specific Request but cannot. It is possible that this call was invoked outside of a React component. If you are calling it from within a React component that is an async function after the first `await` then you are in an environment which does not support AsyncLocalStorage. In this kind of environment ReactDOM.preload() does not do anything when called in an async manner. Try moving this function call above the first `await` within the component or remove this call. In environments that support AsyncLocalStorage such as Node.js you can call this method anywhere in a React component even after `await` operator.',
+      {withoutStack: true},
+    );
+
+    const container = document.createElement('div');
+    const root = ReactDOMClient.createRoot(container);
+    await act(() => {
+      root.render(<App />);
+    });
+    expect(document.head.innerHTML).toBe(
+      '<link href="before" rel="preload" as="style">',
+    );
+    expect(container.innerHTML).toBe('<p>hello world</p>');
+  });
+
+  it('Does not support Float directives in server components anywhere in Fizz', async () => {
+    // In environments that do not support AsyncLocalStorage the Flight client has no ability
+    // to scope directive dispatching to a specific Request. In Fiber this isn't a problem because
+    // the Browser scope acts like a singleton and we can dispatch away. But in Fizz we need to have
+    // a reference to Resources and this is only possible during render unless you support AsyncLocalStorage.
+    function Component() {
+      return <p>hello world</p>;
+    }
+
+    const ClientComponent = clientExports(Component);
+
+    async function ServerComponent() {
+      ReactDOM.preload('before', {as: 'style'});
+      await 1;
+      ReactDOM.preload('after', {as: 'style'});
+      return <ClientComponent />;
+    }
+
+    const stream = ReactServerDOMServer.renderToReadableStream(
+      <ServerComponent />,
+      webpackMap,
+    );
+
+    let response = null;
+    function getResponse() {
+      if (response === null) {
+        response = ReactServerDOMClient.createFromReadableStream(stream);
+      }
+      return response;
+    }
+
+    function App() {
+      return (
+        <html>
+          <body>{getResponse()}</body>
+        </html>
+      );
+    }
+
+    // pausing to let Flight runtime tick. This is a test only artifact of the fact that
+    // we aren't operating separate module graphs for flight and fiber. In a real app
+    // each would have their own dispatcher and there would be no cross dispatching.
+    await expect(async () => {
+      await 1;
+    }).toErrorDev(
+      'ReactDOM.preload(): React expected to be able to associate this call to a specific Request but cannot. It is possible that this call was invoked outside of a React component. If you are calling it from within a React component that is an async function after the first `await` then you are in an environment which does not support AsyncLocalStorage. In this kind of environment ReactDOM.preload() does not do anything when called in an async manner. Try moving this function call above the first `await` within the component or remove this call. In environments that support AsyncLocalStorage such as Node.js you can call this method anywhere in a React component even after `await` operator.',
+      {withoutStack: true},
+    );
+
+    let fizzStream;
+    await act(async () => {
+      fizzStream = await ReactDOMFizzServer.renderToReadableStream(<App />);
+    });
+
+    const decoder = new TextDecoder();
+    const reader = fizzStream.getReader();
+    let content = '';
+    while (true) {
+      const {done, value} = await reader.read();
+      if (done) {
+        content += decoder.decode();
+        break;
+      }
+      content += decoder.decode(value, {stream: true});
+    }
+
+    expect(content).toEqual(
+      '<!DOCTYPE html><html><head>' +
+        '</head><body><p>hello world</p></body></html>',
+    );
+  });
 });
diff --git a/packages/react-server-native-relay/src/ReactFlightClientConfigNativeRelay.js b/packages/react-server-native-relay/src/ReactFlightClientConfigNativeRelay.js
index e21df4d13e80c..75bb6d66d9d00 100644
--- a/packages/react-server-native-relay/src/ReactFlightClientConfigNativeRelay.js
+++ b/packages/react-server-native-relay/src/ReactFlightClientConfigNativeRelay.js
@@ -95,3 +95,5 @@ const dummy = {};
 export function parseModel<T>(response: Response, json: UninitializedModel): T {
   return (parseModelRecursively(response, dummy, '', json): any);
 }
+
+export function dispatchDirective(payload: mixed) {}
diff --git a/packages/react-server-native-relay/src/ReactFlightServerConfigNativeRelay.js b/packages/react-server-native-relay/src/ReactFlightServerConfigNativeRelay.js
index ab815ae2f0144..10c697ef9fa0c 100644
--- a/packages/react-server-native-relay/src/ReactFlightServerConfigNativeRelay.js
+++ b/packages/react-server-native-relay/src/ReactFlightServerConfigNativeRelay.js
@@ -8,6 +8,7 @@
  */
 
 import type {RowEncoding, JSONValue} from './ReactFlightNativeRelayProtocol';
+import type {Directive} from 'react-native-renderer/src/server/ReactFlightServerConfigNative';
 import type {
   Request,
   ReactClientValue,
@@ -187,6 +188,16 @@ export function processImportChunk(
   return ['I', id, clientReferenceMetadata];
 }
 
+export function processDirectiveChunk(
+  request: Request,
+  id: number,
+  payload: ReactClientValue,
+): Chunk {
+  throw new Error(
+    'React Internal Error: processDirectiveChunk is not implemented for Native-Relay. The fact that this method was called means there is a but in React.',
+  );
+}
+
 export function scheduleWork(callback: () => void) {
   callback();
 }
@@ -194,8 +205,10 @@ export function scheduleWork(callback: () => void) {
 export function flushBuffered(destination: Destination) {}
 
 export const supportsRequestStorage = false;
-export const requestStorage: AsyncLocalStorage<Map<Function, mixed>> =
-  (null: any);
+export const requestStorage: AsyncLocalStorage<{
+  cache: Map<Function, mixed>,
+  directives: Array<Directive>,
+}> = (null: any);
 
 export function beginWriting(destination: Destination) {}
 
diff --git a/packages/react-server/src/ReactFizzResources.js b/packages/react-server/src/ReactFizzResources.js
new file mode 100644
index 0000000000000..ba5da2a155b0d
--- /dev/null
+++ b/packages/react-server/src/ReactFizzResources.js
@@ -0,0 +1,35 @@
+/**
+ * Copyright (c) Meta Platforms, Inc. and affiliates.
+ *
+ * This source code is licensed under the MIT license found in the
+ * LICENSE file in the root directory of this source tree.
+ *
+ * @flow
+ */
+
+import type {Resources} from './ReactFizzConfig';
+
+import {
+  supportsRequestStorage,
+  requestStorage2,
+} from './ReactServerStreamConfig';
+
+export function resolveResources(): null | Resources {
+  if (currentResources) return currentResources;
+  if (supportsRequestStorage) {
+    const store = requestStorage2.getStore();
+    return store || null;
+  }
+  return null;
+}
+
+let currentResources: null | Resources = null;
+
+export function setCurrentResources(store: null | Resources): null | Resources {
+  currentResources = store;
+  return currentResources;
+}
+
+export function getCurrentResources(): null | Resources {
+  return currentResources;
+}
diff --git a/packages/react-server/src/ReactFizzServer.js b/packages/react-server/src/ReactFizzServer.js
index eab8c6c50e366..7bbcaa8621e0c 100644
--- a/packages/react-server/src/ReactFizzServer.js
+++ b/packages/react-server/src/ReactFizzServer.js
@@ -42,6 +42,8 @@ import {
   flushBuffered,
   close,
   closeWithError,
+  supportsRequestStorage,
+  requestStorage2,
 } from './ReactServerStreamConfig';
 import {
   writeCompletedRoot,
@@ -76,6 +78,7 @@ import {
   setCurrentlyRenderingBoundaryResourcesTarget,
   createResources,
   createBoundaryResources,
+  prepareHostDispatcher,
 } from './ReactFizzConfig';
 import {
   constructClassInstance,
@@ -277,6 +280,7 @@ export function createRequest(
   onShellError: void | ((error: mixed) => void),
   onFatalError: void | ((error: mixed) => void),
 ): Request {
+  prepareHostDispatcher();
   const pingedTasks: Array<Task> = [];
   const abortSet: Set<Task> = new Set();
   const resources: Resources = createResources();
@@ -1947,7 +1951,7 @@ export function performWork(request: Request): void {
     ReactCurrentCache.current = DefaultCacheDispatcher;
   }
 
-  const previousHostDispatcher = prepareToRender(request.resources);
+  prepareToRender(request.resources);
   let prevGetCurrentStackImpl;
   if (__DEV__) {
     prevGetCurrentStackImpl = ReactDebugCurrentFrame.getCurrentStack;
@@ -1975,7 +1979,7 @@ export function performWork(request: Request): void {
     if (enableCache) {
       ReactCurrentCache.current = prevCacheDispatcher;
     }
-    cleanupAfterRender(previousHostDispatcher);
+    cleanupAfterRender();
 
     if (__DEV__) {
       ReactDebugCurrentFrame.getCurrentStack = prevGetCurrentStackImpl;
@@ -2411,7 +2415,13 @@ function flushCompletedQueues(
 }
 
 export function startWork(request: Request): void {
-  scheduleWork(() => performWork(request));
+  if (supportsRequestStorage) {
+    scheduleWork(() =>
+      requestStorage2.run(request.resources, performWork, request),
+    );
+  } else {
+    scheduleWork(() => performWork(request));
+  }
 }
 
 export function startFlowing(request: Request, destination: Destination): void {
diff --git a/packages/react-server/src/ReactFlightCache.js b/packages/react-server/src/ReactFlightCache.js
index 7ac8aaa66222f..589d0984d09ab 100644
--- a/packages/react-server/src/ReactFlightCache.js
+++ b/packages/react-server/src/ReactFlightCache.js
@@ -21,8 +21,8 @@ function createSignal(): AbortSignal {
 function resolveCache(): Map<Function, mixed> {
   if (currentCache) return currentCache;
   if (supportsRequestStorage) {
-    const cache = requestStorage.getStore();
-    if (cache) return cache;
+    const store = requestStorage.getStore();
+    if (store) return store.cache;
   }
   // Since we override the dispatcher all the time, we're effectively always
   // active and so to support cache() and fetch() outside of render, we yield
diff --git a/packages/react-server/src/ReactFlightDirectives.js b/packages/react-server/src/ReactFlightDirectives.js
new file mode 100644
index 0000000000000..898d8f7912c3d
--- /dev/null
+++ b/packages/react-server/src/ReactFlightDirectives.js
@@ -0,0 +1,38 @@
+/**
+ * Copyright (c) Meta Platforms, Inc. and affiliates.
+ *
+ * This source code is licensed under the MIT license found in the
+ * LICENSE file in the root directory of this source tree.
+ *
+ * @flow
+ */
+
+import type {Directive} from './ReactFlightServerConfig';
+import {
+  supportsRequestStorage,
+  requestStorage,
+} from './ReactFlightServerConfig';
+
+export function resolveDirectives(): null | Array<Directive> {
+  if (currentDirectives) return currentDirectives;
+  if (supportsRequestStorage) {
+    const store = requestStorage.getStore();
+    if (store) return store.directives;
+  }
+  // If we do not have a store with directives we can't resolve them.
+  // Callers need to handle cases where directives are unavailable
+  return null;
+}
+
+let currentDirectives: null | Array<Directive> = null;
+
+export function setCurrentDirectives(
+  directives: null | Array<Directive>,
+): null | Array<Directive> {
+  currentDirectives = directives;
+  return currentDirectives;
+}
+
+export function getCurrentDirectives(): null | Array<Directive> {
+  return currentDirectives;
+}
diff --git a/packages/react-server/src/ReactFlightServer.js b/packages/react-server/src/ReactFlightServer.js
index 1c127c886b7be..e00366dfe3122 100644
--- a/packages/react-server/src/ReactFlightServer.js
+++ b/packages/react-server/src/ReactFlightServer.js
@@ -16,6 +16,7 @@ import type {
   ClientReferenceKey,
   ServerReference,
   ServerReferenceId,
+  Directive,
 } from './ReactFlightServerConfig';
 import type {ContextSnapshot} from './ReactFlightNewContext';
 import type {ThenableState} from './ReactFlightThenable';
@@ -44,6 +45,7 @@ import {
   processErrorChunkProd,
   processErrorChunkDev,
   processReferenceChunk,
+  processDirectiveChunk,
   resolveClientReferenceMetadata,
   getServerReferenceId,
   getServerReferenceBoundArguments,
@@ -52,6 +54,7 @@ import {
   isServerReference,
   supportsRequestStorage,
   requestStorage,
+  prepareHostDispatcher,
 } from './ReactFlightServerConfig';
 
 import {
@@ -66,6 +69,10 @@ import {
   getCurrentCache,
   setCurrentCache,
 } from './ReactFlightCache';
+import {
+  getCurrentDirectives,
+  setCurrentDirectives,
+} from './ReactFlightDirectives';
 import {
   pushProvider,
   popProvider,
@@ -146,17 +153,23 @@ type Task = {
   thenableState: ThenableState | null,
 };
 
+type Store = {
+  cache: Map<Function, mixed>,
+  directives: Array<Directive>,
+};
+
 export type Request = {
   status: 0 | 1 | 2,
   fatalError: mixed,
   destination: null | Destination,
   bundlerConfig: ClientManifest,
-  cache: Map<Function, mixed>,
+  store: Store,
   nextChunkId: number,
   pendingChunks: number,
   abortableTasks: Set<Task>,
   pingedTasks: Array<Task>,
   completedImportChunks: Array<Chunk>,
+  completedDirectiveChunks: Array<Chunk>,
   completedJSONChunks: Array<Chunk>,
   completedErrorChunks: Array<Chunk>,
   writtenSymbols: Map<symbol, number>,
@@ -196,6 +209,7 @@ export function createRequest(
       'Currently React only supports one RSC renderer at a time.',
     );
   }
+  prepareHostDispatcher();
   ReactCurrentCache.current = DefaultCacheDispatcher;
 
   const abortSet: Set<Task> = new Set();
@@ -205,12 +219,16 @@ export function createRequest(
     fatalError: null,
     destination: null,
     bundlerConfig,
-    cache: new Map(),
+    store: {
+      cache: new Map(),
+      directives: [],
+    },
     nextChunkId: 0,
     pendingChunks: 0,
     abortableTasks: abortSet,
     pingedTasks: pingedTasks,
     completedImportChunks: ([]: Array<Chunk>),
+    completedDirectiveChunks: ([]: Array<Chunk>),
     completedJSONChunks: ([]: Array<Chunk>),
     completedErrorChunks: ([]: Array<Chunk>),
     writtenSymbols: new Map(),
@@ -1038,6 +1056,15 @@ function emitImportChunk(
   request.completedImportChunks.push(processedChunk);
 }
 
+function emitDirectiveChunk(request: Request, directive: Directive): void {
+  const processedChunk = processDirectiveChunk(
+    request,
+    request.nextChunkId++,
+    directive,
+  );
+  request.completedDirectiveChunks.push(processedChunk);
+}
+
 function emitSymbolChunk(request: Request, id: number, name: string): void {
   const symbolReference = serializeSymbolReference(name);
   const processedChunk = processReferenceChunk(request, id, symbolReference);
@@ -1146,6 +1173,12 @@ function retryTask(request: Request, task: Task): void {
         emitErrorChunkProd(request, task.id, digest);
       }
     }
+  } finally {
+    const directives = request.store.directives;
+    for (let i = 0; i < directives.length; i++) {
+      emitDirectiveChunk(request, directives[i]);
+    }
+    directives.length = 0;
   }
 }
 
@@ -1153,7 +1186,9 @@ function performWork(request: Request): void {
   const prevDispatcher = ReactCurrentDispatcher.current;
   const prevCache = getCurrentCache();
   ReactCurrentDispatcher.current = HooksDispatcher;
-  setCurrentCache(request.cache);
+  setCurrentCache(request.store.cache);
+  const prevDirectives = getCurrentDirectives();
+  setCurrentDirectives(request.store.directives);
   prepareToUseHooksForRequest(request);
 
   try {
@@ -1172,6 +1207,7 @@ function performWork(request: Request): void {
   } finally {
     ReactCurrentDispatcher.current = prevDispatcher;
     setCurrentCache(prevCache);
+    setCurrentDirectives(prevDirectives);
     resetHooksForRequest();
   }
 }
@@ -1206,6 +1242,26 @@ function flushCompletedChunks(
       }
     }
     importsChunks.splice(0, i);
+    // Next comes directives data.
+    if (__DEV__) {
+      if (request.store.directives.length > 0) {
+        console.error(
+          'Internal React Error: React expected all directives to have been processed before writing any but it encountered unprocessed directives. Please file an issue.',
+        );
+      }
+    }
+    const directiveChunks = request.completedDirectiveChunks;
+    i = 0;
+    for (; i < directiveChunks.length; i++) {
+      const chunk = directiveChunks[i];
+      const keepWriting: boolean = writeChunkAndReturn(destination, chunk);
+      if (!keepWriting) {
+        request.destination = null;
+        i++;
+        break;
+      }
+    }
+    directiveChunks.splice(0, i);
     // Next comes model data.
     const jsonChunks = request.completedJSONChunks;
     i = 0;
@@ -1248,7 +1304,7 @@ function flushCompletedChunks(
 
 export function startWork(request: Request): void {
   if (supportsRequestStorage) {
-    scheduleWork(() => requestStorage.run(request.cache, performWork, request));
+    scheduleWork(() => requestStorage.run(request.store, performWork, request));
   } else {
     scheduleWork(() => performWork(request));
   }
diff --git a/packages/react-server/src/ReactFlightServerConfigBundlerCustom.js b/packages/react-server/src/ReactFlightServerConfigBundlerCustom.js
index e11c154d05f32..b1fbc93ee61b1 100644
--- a/packages/react-server/src/ReactFlightServerConfigBundlerCustom.js
+++ b/packages/react-server/src/ReactFlightServerConfigBundlerCustom.js
@@ -23,3 +23,4 @@ export const resolveClientReferenceMetadata =
 export const getServerReferenceId = $$$config.getServerReferenceId;
 export const getServerReferenceBoundArguments =
   $$$config.getServerReferenceBoundArguments;
+export const prepareHostDispatcher = $$$config.prepareHostDispatcher;
diff --git a/packages/react-server/src/ReactFlightServerConfigStream.js b/packages/react-server/src/ReactFlightServerConfigStream.js
index 4377a313b374a..70ba32d1ce83e 100644
--- a/packages/react-server/src/ReactFlightServerConfigStream.js
+++ b/packages/react-server/src/ReactFlightServerConfigStream.js
@@ -156,6 +156,17 @@ export function processImportChunk(
   return stringToChunk(row);
 }
 
+export function processDirectiveChunk(
+  request: Request,
+  id: number,
+  payload: ReactClientValue,
+): Chunk {
+  // $FlowFixMe[incompatible-type] stringify can return null
+  const json: string = stringify(payload, request.toJSON);
+  const row = serializeRowHeader('D', id) + json + '\n';
+  return stringToChunk(row);
+}
+
 export {
   scheduleWork,
   flushBuffered,
diff --git a/packages/react-server/src/ReactServerStreamConfigBrowser.js b/packages/react-server/src/ReactServerStreamConfigBrowser.js
index aa9cac7b2c373..877ce6ef9980a 100644
--- a/packages/react-server/src/ReactServerStreamConfigBrowser.js
+++ b/packages/react-server/src/ReactServerStreamConfigBrowser.js
@@ -7,6 +7,8 @@
  * @flow
  */
 
+import type {Resources} from './ReactFizzConfig';
+
 export type Destination = ReadableStreamController;
 
 export type PrecomputedChunk = Uint8Array;
@@ -22,8 +24,11 @@ export function flushBuffered(destination: Destination) {
 }
 
 export const supportsRequestStorage = false;
-export const requestStorage: AsyncLocalStorage<Map<Function, mixed>> =
-  (null: any);
+export const requestStorage: AsyncLocalStorage<{
+  cache: Map<Function, mixed>,
+  directives: Array<string>,
+}> = (null: any);
+export const requestStorage2: AsyncLocalStorage<Resources> = (null: any);
 
 const VIEW_SIZE = 512;
 let currentView = null;
diff --git a/packages/react-server/src/ReactServerStreamConfigBun.js b/packages/react-server/src/ReactServerStreamConfigBun.js
index 9cc88c4086475..cf1c3d95a6a8f 100644
--- a/packages/react-server/src/ReactServerStreamConfigBun.js
+++ b/packages/react-server/src/ReactServerStreamConfigBun.js
@@ -7,6 +7,8 @@
  * @flow
  */
 
+import type {Resources} from './ReactFizzConfig';
+
 type BunReadableStreamController = ReadableStreamController & {
   end(): mixed,
   write(data: Chunk): void,
@@ -28,7 +30,11 @@ export function flushBuffered(destination: Destination) {
 
 // AsyncLocalStorage is not available in bun
 export const supportsRequestStorage = false;
-export const requestStorage = (null: any);
+export const requestStorage: AsyncLocalStorage<{
+  cache: Map<Function, mixed>,
+  directives: Array<string>,
+}> = (null: any);
+export const requestStorage2: AsyncLocalStorage<Resources> = (null: any);
 
 export function beginWriting(destination: Destination) {}
 
diff --git a/packages/react-server/src/ReactServerStreamConfigEdge.js b/packages/react-server/src/ReactServerStreamConfigEdge.js
index db6bfb14fee8b..c8065bfbd0a4d 100644
--- a/packages/react-server/src/ReactServerStreamConfigEdge.js
+++ b/packages/react-server/src/ReactServerStreamConfigEdge.js
@@ -7,6 +7,8 @@
  * @flow
  */
 
+import type {Resources} from './ReactFizzConfig';
+
 export type Destination = ReadableStreamController;
 
 export type PrecomputedChunk = Uint8Array;
@@ -23,7 +25,11 @@ export function flushBuffered(destination: Destination) {
 
 // For now, we get this from the global scope, but this will likely move to a module.
 export const supportsRequestStorage = typeof AsyncLocalStorage === 'function';
-export const requestStorage: AsyncLocalStorage<Map<Function, mixed>> =
+export const requestStorage: AsyncLocalStorage<{
+  cache: Map<Function, mixed>,
+  directives: Array<string>,
+}> = supportsRequestStorage ? new AsyncLocalStorage() : (null: any);
+export const requestStorage2: AsyncLocalStorage<Resources> =
   supportsRequestStorage ? new AsyncLocalStorage() : (null: any);
 
 const VIEW_SIZE = 512;
diff --git a/packages/react-server/src/ReactServerStreamConfigNode.js b/packages/react-server/src/ReactServerStreamConfigNode.js
index 5d33ce7d6576d..79e01ab2430f1 100644
--- a/packages/react-server/src/ReactServerStreamConfigNode.js
+++ b/packages/react-server/src/ReactServerStreamConfigNode.js
@@ -8,6 +8,9 @@
  */
 
 import type {Writable} from 'stream';
+import type {Directive} from './ReactFlightServerConfig';
+import type {Resources} from './ReactFizzConfig';
+
 import {TextEncoder} from 'util';
 import {AsyncLocalStorage} from 'async_hooks';
 
@@ -34,8 +37,17 @@ export function flushBuffered(destination: Destination) {
   }
 }
 
+// Conceptually we don't need two request storages because should have
+// separate modules graphs for Flight and Fizz and we could type the store
+// for the runtime. However, for testing and typing it is simpler to just
+// have two stores. I am calling the second one requestStorage2 to hint
+// that it is not not inherent that there is a Fizz storage and a Flight storage.
 export const supportsRequestStorage = true;
-export const requestStorage: AsyncLocalStorage<Map<Function, mixed>> =
+export const requestStorage: AsyncLocalStorage<{
+  cache: Map<Function, mixed>,
+  directives: Array<Directive>,
+}> = new AsyncLocalStorage();
+export const requestStorage2: AsyncLocalStorage<Resources> =
   new AsyncLocalStorage();
 
 const VIEW_SIZE = 2048;
diff --git a/packages/react-server/src/forks/ReactFizzConfig.custom.js b/packages/react-server/src/forks/ReactFizzConfig.custom.js
index f761eb392f3c0..bbc567e07c1b1 100644
--- a/packages/react-server/src/forks/ReactFizzConfig.custom.js
+++ b/packages/react-server/src/forks/ReactFizzConfig.custom.js
@@ -68,6 +68,7 @@ export const writeCompletedBoundaryInstruction =
   $$$config.writeCompletedBoundaryInstruction;
 export const writeClientRenderBoundaryInstruction =
   $$$config.writeClientRenderBoundaryInstruction;
+export const prepareHostDispatcher = $$$config.prepareHostDispatcher;
 export const prepareToRender = $$$config.prepareToRender;
 export const cleanupAfterRender = $$$config.cleanupAfterRender;
 
diff --git a/packages/react-server/src/forks/ReactFlightServerConfig.custom.js b/packages/react-server/src/forks/ReactFlightServerConfig.custom.js
index 28977b2357cc6..e94f62177f621 100644
--- a/packages/react-server/src/forks/ReactFlightServerConfig.custom.js
+++ b/packages/react-server/src/forks/ReactFlightServerConfig.custom.js
@@ -10,4 +10,6 @@
 export * from '../ReactFlightServerConfigStream';
 export * from '../ReactFlightServerConfigBundlerCustom';
 
+export type Directive = void;
 export const isPrimaryRenderer = false;
+export const prepareHostDispatcher = () => {};
diff --git a/packages/react-server/src/forks/ReactServerStreamConfig.custom.js b/packages/react-server/src/forks/ReactServerStreamConfig.custom.js
index ed00afa434e7e..924de630bddbf 100644
--- a/packages/react-server/src/forks/ReactServerStreamConfig.custom.js
+++ b/packages/react-server/src/forks/ReactServerStreamConfig.custom.js
@@ -37,6 +37,7 @@ export const completeWriting = $$$config.completeWriting;
 export const flushBuffered = $$$config.flushBuffered;
 export const supportsRequestStorage = $$$config.supportsRequestStorage;
 export const requestStorage = $$$config.requestStorage;
+export const requestStorage2 = $$$config.requestStorage2;
 export const close = $$$config.close;
 export const closeWithError = $$$config.closeWithError;
 export const stringToChunk = $$$config.stringToChunk;
diff --git a/scripts/error-codes/codes.json b/scripts/error-codes/codes.json
index d48354c974202..c2d5851c99916 100644
--- a/scripts/error-codes/codes.json
+++ b/scripts/error-codes/codes.json
@@ -460,5 +460,6 @@
   "472": "Type %s is not supported as an argument to a Server Function.",
   "473": "React doesn't accept base64 encoded file uploads because we don't except form data passed from a browser to ever encode data that way. If that's the wrong assumption, we can easily fix it.",
   "474": "Suspense Exception: This is not a real error, and should not leak into userspace. If you're seeing this, it's likely a bug in React.",
-  "475": "Internal React Error: suspendedState null when it was expected to exists. Please report this as a React bug."
+  "475": "Internal React Error: suspendedState null when it was expected to exists. Please report this as a React bug.",
+  "476": "React Internal Error: processDirectiveChunk is not implemented for Native-Relay. The fact that this method was called means there is a but in React."
 }