diff --git a/.changeset/mean-jars-count.md b/.changeset/mean-jars-count.md
new file mode 100644
index 000000000000..e0d567e5195e
--- /dev/null
+++ b/.changeset/mean-jars-count.md
@@ -0,0 +1,5 @@
+---
+"wrangler": minor
+---
+
+Add support for Workers AI in local mode
diff --git a/fixtures/ai-app/.gitignore b/fixtures/ai-app/.gitignore
new file mode 100644
index 000000000000..1521c8b7652b
--- /dev/null
+++ b/fixtures/ai-app/.gitignore
@@ -0,0 +1 @@
+dist
diff --git a/fixtures/ai-app/package.json b/fixtures/ai-app/package.json
new file mode 100644
index 000000000000..c2b026ebdff2
--- /dev/null
+++ b/fixtures/ai-app/package.json
@@ -0,0 +1,21 @@
+{
+	"name": "ai-app",
+	"version": "1.0.1",
+	"private": true,
+	"description": "",
+	"license": "ISC",
+	"author": "",
+	"main": "src/index.js",
+	"scripts": {
+		"check:type": "tsc",
+		"test": "vitest run",
+		"test:watch": "vitest",
+		"type:tests": "tsc -p ./tests/tsconfig.json"
+	},
+	"devDependencies": {
+		"undici": "^5.23.0",
+		"wrangler": "workspace:*",
+		"@cloudflare/workers-tsconfig": "workspace:^",
+		"@cloudflare/ai": "^1.0.35"
+	}
+}
diff --git a/fixtures/ai-app/src/index.js b/fixtures/ai-app/src/index.js
new file mode 100644
index 000000000000..269f4491906f
--- /dev/null
+++ b/fixtures/ai-app/src/index.js
@@ -0,0 +1,12 @@
+console.log("startup log");
+
+export default {
+	async fetch(request, env) {
+		console.log("request log");
+
+		return Response.json({
+			binding: env.AI,
+			fetcher: env.AI.fetch.toString(),
+		});
+	},
+};
diff --git a/fixtures/ai-app/tests/index.test.ts b/fixtures/ai-app/tests/index.test.ts
new file mode 100644
index 000000000000..472bd2c2790f
--- /dev/null
+++ b/fixtures/ai-app/tests/index.test.ts
@@ -0,0 +1,31 @@
+import { resolve } from "path";
+import { fetch } from "undici";
+import { describe, it, beforeAll, afterAll } from "vitest";
+import { runWranglerDev } from "../../shared/src/run-wrangler-long-lived";
+
+describe("'wrangler dev' correctly renders pages", () => {
+	let ip: string,
+		port: number,
+		stop: (() => Promise<unknown>) | undefined,
+		getOutput: () => string;
+
+	beforeAll(async () => {
+		({ ip, port, stop, getOutput } = await runWranglerDev(
+			resolve(__dirname, ".."),
+			["--local", "--port=0", "--inspector-port=0"]
+		));
+	});
+
+	afterAll(async () => {
+		await stop?.();
+	});
+
+	it("ai binding is defined ", async ({ expect }) => {
+		const response = await fetch(`http://${ip}:${port}/`);
+		const content = await response.json();
+		expect(content).toEqual({
+			binding: {},
+			fetcher: "function fetch() { [native code] }",
+		});
+	});
+});
diff --git a/fixtures/ai-app/tests/tsconfig.json b/fixtures/ai-app/tests/tsconfig.json
new file mode 100644
index 000000000000..d2ce7f144694
--- /dev/null
+++ b/fixtures/ai-app/tests/tsconfig.json
@@ -0,0 +1,7 @@
+{
+	"extends": "@cloudflare/workers-tsconfig/tsconfig.json",
+	"compilerOptions": {
+		"types": ["node"]
+	},
+	"include": ["**/*.ts", "../../../node-types.d.ts"]
+}
diff --git a/fixtures/ai-app/tsconfig.json b/fixtures/ai-app/tsconfig.json
new file mode 100644
index 000000000000..b901134e4e79
--- /dev/null
+++ b/fixtures/ai-app/tsconfig.json
@@ -0,0 +1,13 @@
+{
+	"compilerOptions": {
+		"target": "ES2020",
+		"esModuleInterop": true,
+		"module": "CommonJS",
+		"lib": ["ES2020"],
+		"types": ["node"],
+		"skipLibCheck": true,
+		"moduleResolution": "node",
+		"noEmit": true
+	},
+	"include": ["tests", "../../node-types.d.ts"]
+}
diff --git a/fixtures/ai-app/vitest.config.ts b/fixtures/ai-app/vitest.config.ts
new file mode 100644
index 000000000000..ed02453b1c87
--- /dev/null
+++ b/fixtures/ai-app/vitest.config.ts
@@ -0,0 +1,10 @@
+import { defineConfig } from "vitest/config";
+
+export default defineConfig({
+	test: {
+		testTimeout: 10_000,
+		hookTimeout: 10_000,
+		teardownTimeout: 10_000,
+		useAtomics: true,
+	},
+});
diff --git a/fixtures/ai-app/wrangler.toml b/fixtures/ai-app/wrangler.toml
new file mode 100644
index 000000000000..841585819660
--- /dev/null
+++ b/fixtures/ai-app/wrangler.toml
@@ -0,0 +1,7 @@
+name = "ai-app"
+compatibility_date = "2023-11-21"
+
+main = "src/index.js"
+
+[ai]
+binding = "AI"
diff --git a/packages/wrangler/package.json b/packages/wrangler/package.json
index 8bdc476cf5cf..a7f1b0e45266 100644
--- a/packages/wrangler/package.json
+++ b/packages/wrangler/package.json
@@ -117,6 +117,7 @@
 		"xxhash-wasm": "^1.0.1"
 	},
 	"devDependencies": {
+		"@cloudflare/ai": "^1.0.35",
 		"@cloudflare/cli": "workspace:*",
 		"@cloudflare/eslint-config-worker": "*",
 		"@cloudflare/pages-shared": "workspace:^",
diff --git a/packages/wrangler/src/ai/fetcher.ts b/packages/wrangler/src/ai/fetcher.ts
new file mode 100644
index 000000000000..85c2ce25ebf2
--- /dev/null
+++ b/packages/wrangler/src/ai/fetcher.ts
@@ -0,0 +1,20 @@
+import { Response } from "miniflare";
+import { performApiFetch } from "../cfetch/internal";
+import { getAccountId } from "../user";
+import type { Request } from "miniflare";
+
+export async function AIFetcher(request: Request) {
+	const accountId = await getAccountId();
+
+	request.headers.delete("Host");
+	request.headers.delete("Content-Length");
+
+	const res = await performApiFetch(`/accounts/${accountId}/ai/run/proxy`, {
+		method: "POST",
+		headers: Object.fromEntries(request.headers.entries()),
+		body: request.body,
+		duplex: "half",
+	});
+
+	return new Response(res.body, { status: res.status });
+}
diff --git a/packages/wrangler/src/api/dev.ts b/packages/wrangler/src/api/dev.ts
index 2d55dc595a84..16d4a0a35492 100644
--- a/packages/wrangler/src/api/dev.ts
+++ b/packages/wrangler/src/api/dev.ts
@@ -50,6 +50,9 @@ export interface UnstableDevOptions {
 		bucket_name: string;
 		preview_bucket_name?: string;
 	}[];
+	ai?: {
+		binding: string;
+	};
 	moduleRoot?: string;
 	rules?: Rule[];
 	logLevel?: "none" | "info" | "error" | "log" | "warn" | "debug"; // Specify logging level  [choices: "debug", "info", "log", "warn", "error", "none"] [default: "log"]
diff --git a/packages/wrangler/src/dev.tsx b/packages/wrangler/src/dev.tsx
index b64136ad4dca..5b6b0cfc7631 100644
--- a/packages/wrangler/src/dev.tsx
+++ b/packages/wrangler/src/dev.tsx
@@ -326,6 +326,9 @@ export type AdditionalDevProps = {
 		preview_bucket_name?: string;
 		jurisdiction?: string;
 	}[];
+	ai?: {
+		binding: string;
+	};
 	d1Databases?: Environment["d1_databases"];
 	processEntrypoint?: boolean;
 	additionalModules?: CfModule[];
@@ -832,6 +835,7 @@ function getBindingsAndAssetPaths(args: StartDevOptions, configParam: Config) {
 		r2: args.r2,
 		services: args.services,
 		d1Databases: args.d1Databases,
+		ai: args.ai,
 	});
 
 	const maskedVars = maskVars(bindings, configParam);
@@ -893,7 +897,7 @@ function getBindings(
 		wasm_modules: configParam.wasm_modules,
 		text_blobs: configParam.text_blobs,
 		browser: configParam.browser,
-		ai: configParam.ai,
+		ai: configParam.ai || args.ai,
 		data_blobs: configParam.data_blobs,
 		durable_objects: {
 			bindings: [
diff --git a/packages/wrangler/src/dev/miniflare.ts b/packages/wrangler/src/dev/miniflare.ts
index 8924ed51e6e6..6ae71e549a8b 100644
--- a/packages/wrangler/src/dev/miniflare.ts
+++ b/packages/wrangler/src/dev/miniflare.ts
@@ -2,6 +2,7 @@ import assert from "node:assert";
 import { realpathSync } from "node:fs";
 import path from "node:path";
 import { Log, LogLevel, TypedEventTarget, Mutex, Miniflare } from "miniflare";
+import { AIFetcher } from "../ai/fetcher";
 import { ModuleTypeToRuleType } from "../deployment-bundle/module-collection";
 import { withSourceURLs } from "../deployment-bundle/source-url";
 import { getHttpsOptions } from "../https-options";
@@ -312,6 +313,10 @@ function buildBindingOptions(config: ConfigBundle) {
 				.join("\n"),
 	};
 
+	if (bindings.ai?.binding) {
+		config.serviceBindings[bindings.ai.binding] = AIFetcher;
+	}
+
 	const bindingOptions = {
 		bindings: bindings.vars,
 		textBlobBindings,
@@ -502,13 +507,7 @@ async function buildMiniflareOptions(
 		logger.warn("Miniflare 3 does not support CRON triggers yet, ignoring...");
 	}
 
-	if (config.bindings.ai) {
-		logger.warn(
-			"Workers AI is not currently supported in local mode. Please use --remote to work with it."
-		);
-	}
-
-	if (!config.bindings.ai && config.bindings.vectorize?.length) {
+	if (config.bindings.vectorize?.length) {
 		// TODO: add local support for Vectorize bindings (https://github.com/cloudflare/workers-sdk/issues/4360)
 		logger.warn(
 			"Vectorize bindings are not currently supported in local mode. Please use --remote if you are working with them."
diff --git a/packages/wrangler/src/pages/dev.ts b/packages/wrangler/src/pages/dev.ts
index 2ab0182d2edb..d06e052c6c88 100644
--- a/packages/wrangler/src/pages/dev.ts
+++ b/packages/wrangler/src/pages/dev.ts
@@ -162,6 +162,10 @@ export function Options(yargs: CommonYargsArgv) {
 				type: "array",
 				description: "R2 bucket to bind (--r2 R2_BINDING)",
 			},
+			ai: {
+				type: "string",
+				description: "AI to bind (--ai AI_BINDING)",
+			},
 			service: {
 				type: "array",
 				description: "Service to bind (--service SERVICE=SCRIPT_NAME)",
@@ -222,6 +226,7 @@ export const Handler = async ({
 	do: durableObjects = [],
 	d1: d1s = [],
 	r2: r2s = [],
+	ai,
 	service: requestedServices = [],
 	liveReload,
 	localProtocol,
@@ -677,6 +682,7 @@ export const Handler = async ({
 				return { binding, bucket_name: ref || binding.toString() };
 			})
 			.filter(Boolean) as AdditionalDevProps["r2"],
+		ai: ai ? { binding: ai.toString() } : undefined,
 		rules: usingWorkerDirectory
 			? [
 					{
diff --git a/pnpm-lock.yaml b/pnpm-lock.yaml
index 93fe639358fc..c093aec524fa 100644
--- a/pnpm-lock.yaml
+++ b/pnpm-lock.yaml
@@ -100,6 +100,21 @@ importers:
         specifier: workspace:*
         version: link:../../packages/wrangler
 
+  fixtures/ai-app:
+    devDependencies:
+      '@cloudflare/ai':
+        specifier: ^1.0.35
+        version: 1.0.35
+      '@cloudflare/workers-tsconfig':
+        specifier: workspace:^
+        version: link:../../packages/workers-tsconfig
+      undici:
+        specifier: ^5.23.0
+        version: 5.23.0
+      wrangler:
+        specifier: workspace:*
+        version: link:../../packages/wrangler
+
   fixtures/d1-worker-app:
     devDependencies:
       wrangler:
@@ -1263,6 +1278,9 @@ importers:
         specifier: ~2.3.2
         version: 2.3.2
     devDependencies:
+      '@cloudflare/ai':
+        specifier: ^1.0.35
+        version: 1.0.35
       '@cloudflare/cli':
         specifier: workspace:*
         version: link:../cli
@@ -3273,6 +3291,10 @@ packages:
     bundledDependencies:
       - is-unicode-supported
 
+  /@cloudflare/ai@1.0.35:
+    resolution: {integrity: sha512-lqH62H3vwWxH3ZT8BD5N2Y+a2P9rwWiqtJsJsHFjv5p58aXxk3DJuQpFO1YIqdYUQkJr7QQwKa2HXOOJrjvqhQ==}
+    dev: true
+
   /@cloudflare/cloudflare-brand-assets@4.7.7:
     resolution: {integrity: sha512-L4EqYWkvse0265YIzraYUlkvvjW7Cr5LELiAiBStctENBoqRhMuR4Ff2X4g/r1BwsQ7S0LTECwLLbM6BNzhv3g==}
     dev: true