diff --git a/CHANGELOG.md b/CHANGELOG.md
index b1e01532047..25bff018be2 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -1,3 +1,4 @@
+- Fixed an issue where Cloud Run rewrites in the Hosting emulator would always hit the live Cloud Run API instead of routing to the local functions emulator. (#10588)
 - Updated the Firebase Data Connect local toolkit to v3.4.11, which includes the following changes:
   - [changed] Updated the Golang dependency version to 1.25.11.
 - Fixed issue where `apptesting:execute` command rejects documented `--test-username`, `--test-password`, and `--test-password-file` options.
diff --git a/src/hosting/cloudRunProxy.spec.ts b/src/hosting/cloudRunProxy.spec.ts
index 75e21819372..aa88a8bc8bc 100644
--- a/src/hosting/cloudRunProxy.spec.ts
+++ b/src/hosting/cloudRunProxy.spec.ts
@@ -6,16 +6,21 @@ import * as supertest from "supertest";
 
 import { cloudRunApiOrigin } from "../api";
 import cloudRunProxy, { CloudRunProxyOptions, CloudRunProxyRewrite } from "./cloudRunProxy";
+import { EmulatorRegistry } from "../emulator/registry";
+import { Emulators } from "../emulator/types";
+import { FakeEmulator } from "../emulator/testing/fakeEmulator";
 
 describe("cloudRunProxy", () => {
   const fakeOptions: CloudRunProxyOptions = {
     project: "project-foo",
+    targets: [],
   };
   const fakeRewrite: CloudRunProxyRewrite = { run: { serviceId: "helloworld" } };
   const cloudRunServiceOrigin = "https://helloworld-hash-uc.a.run.app";
 
-  afterEach(() => {
+  afterEach(async () => {
     nock.cleanAll();
+    await EmulatorRegistry.stopAll();
   });
 
   it("should error when not provided a valid Cloud Run service ID", async () => {
@@ -330,4 +335,52 @@ describe("cloudRunProxy", () => {
         expect(spyMw.calledOnce).to.be.true;
       });
   });
+
+  it("should route to the local functions emulator when targets includes 'functions'", async () => {
+    const fakeFunctionsEmulator = new FakeEmulator(Emulators.FUNCTIONS, [
+      { address: "127.0.0.1", family: "IPv4", port: 7778 },
+    ]);
+    await EmulatorRegistry.start(fakeFunctionsEmulator);
+
+    nock("http://127.0.0.1:7778")
+      .get("/project-foo/us-central1/helloworld/")
+      .reply(200, "local version");
+
+    const options: CloudRunProxyOptions = { ...fakeOptions, targets: ["functions"] };
+
+    const mwGenerator = cloudRunProxy(options);
+    const mw = await mwGenerator(fakeRewrite);
+    const spyMw = sinon.spy(mw);
+
+    return supertest(spyMw)
+      .get("/")
+      .expect(200, "local version")
+      .then(() => {
+        expect(spyMw.calledOnce).to.be.true;
+      });
+  });
+
+  it("should route to the local functions emulator in another region", async () => {
+    const fakeFunctionsEmulator = new FakeEmulator(Emulators.FUNCTIONS, [
+      { address: "127.0.0.1", family: "IPv4", port: 7778 },
+    ]);
+    await EmulatorRegistry.start(fakeFunctionsEmulator);
+
+    nock("http://127.0.0.1:7778")
+      .get("/project-foo/asia-southeast1/helloworld/")
+      .reply(200, "local version");
+
+    const options: CloudRunProxyOptions = { ...fakeOptions, targets: ["functions"] };
+
+    const mwGenerator = cloudRunProxy(options);
+    const mw = await mwGenerator({ run: { serviceId: "helloworld", region: "asia-southeast1" } });
+    const spyMw = sinon.spy(mw);
+
+    return supertest(spyMw)
+      .get("/")
+      .expect(200, "local version")
+      .then(() => {
+        expect(spyMw.calledOnce).to.be.true;
+      });
+  });
 });
diff --git a/src/hosting/cloudRunProxy.ts b/src/hosting/cloudRunProxy.ts
index c0bbb7ccb2b..dde3aa0d162 100644
--- a/src/hosting/cloudRunProxy.ts
+++ b/src/hosting/cloudRunProxy.ts
@@ -6,9 +6,13 @@ import { errorRequestHandler, proxyRequestHandler } from "./proxy";
 import { FirebaseError } from "../error";
 import { logger } from "../logger";
 import { needProjectId } from "../projectUtils";
+import { EmulatorRegistry } from "../emulator/registry";
+import { Emulators } from "../emulator/types";
+import { FunctionsEmulator } from "../emulator/functionsEmulator";
 
 export interface CloudRunProxyOptions {
   project?: string;
+  targets?: string[];
 }
 
 export interface CloudRunProxyRewrite {
@@ -70,6 +74,17 @@ export default function (
     logger.info(`[hosting] Cloud Run rewrite ${JSON.stringify(rewrite)} triggered`);
 
     const textIdentifier = `Cloud Run service "${rewrite.run.serviceId}" for region "${rewrite.run.region}"`;
+
+    if (options.targets?.includes("functions") && EmulatorRegistry.isRunning(Emulators.FUNCTIONS)) {
+      const projectId = needProjectId(options);
+      const url = FunctionsEmulator.getHttpFunctionUrl(
+        projectId,
+        rewrite.run.serviceId,
+        rewrite.run.region,
+      );
+      return proxyRequestHandler(url, `local ${textIdentifier}`);
+    }
+
     return getCloudRunUrl(rewrite, needProjectId(options))
       .then((url) => proxyRequestHandler(url, textIdentifier))
       .catch(errorRequestHandler);