diff --git a/core/src/cloud/api.ts b/core/src/cloud/api.ts
index 0073a77fcc..3fdadae3f1 100644
--- a/core/src/cloud/api.ts
+++ b/core/src/cloud/api.ts
@@ -631,7 +631,7 @@ export class CloudApi {
     sessionId: string
     projectId: string
     commandInfo: CommandInfo
-    localServerPort?: number
+    localServerPort: number | undefined
     environment: string
     namespace: string
     isDevCommand: boolean
diff --git a/core/src/commands/base.ts b/core/src/commands/base.ts
index 0f16c7115c..aa27ba49c9 100644
--- a/core/src/commands/base.ts
+++ b/core/src/commands/base.ts
@@ -317,7 +317,8 @@ export abstract class Command<
             sessionId: garden.sessionId,
             projectId: garden.projectId,
             commandInfo: garden.commandInfo,
-            localServerPort: server?.port,
+            // localServerPort only needs to be set for dev/serve commands
+            localServerPort: undefined,
             environment: garden.environmentName,
             namespace: garden.namespace,
             isDevCommand: garden.commandInfo.name === "dev",
diff --git a/core/src/commands/serve.ts b/core/src/commands/serve.ts
index 8bb55d1115..8e2b2a0794 100644
--- a/core/src/commands/serve.ts
+++ b/core/src/commands/serve.ts
@@ -179,7 +179,7 @@ export class ServeCommand<
           const session = await cloudApi.registerSession({
             parentSessionId: undefined,
             projectId,
-            // Use the process (i.e. parent command) session ID for the serve command session
+            // Use the process (i.e. parent command) session ID for the serve/dev command session
             sessionId: manager.sessionId,
             commandInfo: garden.commandInfo,
             localServerPort: this.server.port,
diff --git a/core/src/server/instance-manager.ts b/core/src/server/instance-manager.ts
index c225fe66ac..38ee99969f 100644
--- a/core/src/server/instance-manager.ts
+++ b/core/src/server/instance-manager.ts
@@ -51,7 +51,7 @@ interface GardenInstanceManagerParams {
   log: Log
   sessionId: string
   plugins: GardenPluginReference[]
-  serveCommand?: ServeCommand
+  serveCommand: ServeCommand
   extraCommands?: Command[]
   defaultOpts?: Partial<GardenOpts>
   cloudApiFactory?: CloudApiFactory
@@ -104,6 +104,7 @@ export class GardenInstanceManager {
     this.defaultOpts = defaultOpts || {}
     this.plugins = plugins
     this.cloudApiFactory = cloudApiFactory || CloudApi.factory
+    this.serveCommand = serveCommand
 
     this.events = new EventBus()
     this.monitors = new MonitorManager(log, this.events)
@@ -381,7 +382,7 @@ export class GardenInstanceManager {
 
     const gardenParams = await resolveGardenParamsPartial(projectRoot, gardenOpts)
 
-    return this.ensureInstance(
+    const garden = await this.ensureInstance(
       log,
       {
         projectRoot,
@@ -391,5 +392,28 @@ export class GardenInstanceManager {
       },
       gardenOpts
     )
+
+    if (cloudApi && garden.projectId && this.serveCommand?.server) {
+      // Ensure cloud session is registered for the domain and server session, since this may not happen on startup
+      // if the command isn't started in a Garden project root. This is a no-op if it's already registered.
+      // FIXME: We still need to rethink on the Cloud side how sessions are scoped
+      await cloudApi.registerSession({
+        parentSessionId: undefined,
+        projectId: garden.projectId,
+        // Use the process (i.e. parent command) session ID for the serve/dev command session
+        sessionId: this.sessionId,
+        commandInfo: garden.commandInfo,
+        // set localServerPort only for dev/serve commands
+        localServerPort:
+          this.serveCommand.server.port && ["dev", "serve"].includes(garden.commandInfo.name)
+            ? this.serveCommand.server.port
+            : undefined,
+        environment: garden.environmentName,
+        namespace: garden.namespace,
+        isDevCommand: true,
+      })
+    }
+
+    return garden
   }
 }