diff --git a/fixtures/react-router-cloudflare/workers/app.ts b/fixtures/react-router-cloudflare/workers/app.ts
index 6d6f86672208..df05b6592566 100644
--- a/fixtures/react-router-cloudflare/workers/app.ts
+++ b/fixtures/react-router-cloudflare/workers/app.ts
@@ -1,4 +1,9 @@
 import { createRequestHandler } from "react-router";
+// @ts-ignore - app files are provided by the react-router template
+import { redirectRequest } from "../app/redirect-url";
+// @todo think about how to make __generated__ typeable
+// @ts-ignore
+import { redirects } from "../app/__generated__/$resources.redirects";
 
 declare module "react-router" {
   export interface AppLoadContext {
@@ -17,6 +22,11 @@ const requestHandler = createRequestHandler(
 
 export default {
   async fetch(request, env, ctx) {
+    const redirectResponse = redirectRequest(request, redirects);
+    if (redirectResponse !== undefined) {
+      return redirectResponse;
+    }
+
     return requestHandler(request, {
       EXCLUDE_FROM_SEARCH: false,
       getDefaultActionResource: undefined,
diff --git a/fixtures/webstudio-cloudflare-template/functions/[[path]].ts b/fixtures/webstudio-cloudflare-template/functions/[[path]].ts
index 943b55594f13..d8de1b18d0d9 100644
--- a/fixtures/webstudio-cloudflare-template/functions/[[path]].ts
+++ b/fixtures/webstudio-cloudflare-template/functions/[[path]].ts
@@ -1,4 +1,9 @@
 import { createPagesFunctionHandler } from "@remix-run/cloudflare-pages";
+// @ts-ignore - app files are provided by the defaults template
+import { redirectRequest } from "../app/redirect-url";
+// @todo think about how to make __generated__ typeable
+// @ts-ignore
+import { redirects } from "../app/__generated__/$resources.redirects";
 
 // eslint-disable-next-line @typescript-eslint/ban-ts-comment
 // @ts-ignore - the server build file is generated by `remix vite:build`
@@ -6,4 +11,13 @@ import * as build from "../build/server";
 
 // eslint-disable-next-line @typescript-eslint/ban-ts-comment
 // @ts-ignore - the server build file is generated by `remix vite:build`
-export const onRequest = createPagesFunctionHandler({ build });
+const requestHandler = createPagesFunctionHandler({ build });
+
+export const onRequest: PagesFunction = (context) => {
+  const redirectResponse = redirectRequest(context.request, redirects);
+  if (redirectResponse !== undefined) {
+    return redirectResponse;
+  }
+
+  return requestHandler(context);
+};
diff --git a/packages/cli/src/cloudflare-redirect-entrypoint.test.ts b/packages/cli/src/cloudflare-redirect-entrypoint.test.ts
new file mode 100644
index 000000000000..34363296a0f6
--- /dev/null
+++ b/packages/cli/src/cloudflare-redirect-entrypoint.test.ts
@@ -0,0 +1,76 @@
+import { describe, expect, test } from "vitest";
+import { mkdir, mkdtemp, readFile, rm, writeFile } from "node:fs/promises";
+import { dirname, join } from "node:path";
+import { pathToFileURL } from "node:url";
+
+const cliRoot = process.cwd();
+
+const writeModule = async (path: string, contents: string) => {
+  await mkdir(dirname(path), { recursive: true });
+  await writeFile(path, contents, "utf8");
+};
+
+const importTempModule = async <Module>(path: string) => {
+  return (await import(
+    `${pathToFileURL(path).href}?test=${crypto.randomUUID()}`
+  )) as Module;
+};
+
+const writeTempApp = async (tempDir: string) => {
+  await writeModule(
+    join(tempDir, "app/redirect-url.ts"),
+    `
+      export const redirectRequest = (request, redirects) => {
+        const pathname = new URL(request.url).pathname;
+        const redirect = redirects.find((redirect) => redirect.old === pathname);
+        if (redirect === undefined) {
+          return;
+        }
+        return new Response(null, {
+          status: redirect.status,
+          headers: { Location: redirect.new },
+        });
+      };
+    `
+  );
+  await writeModule(
+    join(tempDir, "app/__generated__/$resources.redirects.ts"),
+    `export const redirects = [{ old: "/missing", new: "/target", status: 301 }];`
+  );
+
+  await writeModule(
+    join(tempDir, "workers/app.ts"),
+    await readFile(
+      join(cliRoot, "templates/react-router-cloudflare/workers/app.ts"),
+      "utf8"
+    )
+  );
+};
+
+describe("cloudflare redirect entrypoint", () => {
+  test("redirects before unmatched routes reach react-router", async () => {
+    const tempDir = await mkdtemp(join(cliRoot, ".tmp-cloudflare-redirect-"));
+    try {
+      await writeTempApp(tempDir);
+      const worker = await importTempModule<{
+        default: {
+          fetch: (
+            request: Request,
+            env: Record<string, never>,
+            ctx: Record<string, never>
+          ) => Response | Promise<Response>;
+        };
+      }>(join(tempDir, "workers/app.ts"));
+      const response = await worker.default.fetch(
+        new Request("https://example.com/missing"),
+        {},
+        {}
+      );
+
+      expect(response.status).toBe(301);
+      expect(response.headers.get("Location")).toBe("/target");
+    } finally {
+      await rm(tempDir, { recursive: true, force: true });
+    }
+  });
+});
diff --git a/packages/cli/src/redirect-url.test.ts b/packages/cli/src/redirect-url.test.ts
index 67757e6b15a9..d3e667789eaa 100644
--- a/packages/cli/src/redirect-url.test.ts
+++ b/packages/cli/src/redirect-url.test.ts
@@ -85,6 +85,37 @@ describe("redirect-url fixture copies", () => {
       )
     );
   });
+
+  test("keeps react-router-cloudflare worker redirect handling synced with template", async () => {
+    await expect(
+      readFile(
+        join(repoRoot, "fixtures/react-router-cloudflare/workers/app.ts"),
+        "utf8"
+      )
+    ).resolves.toEqual(
+      await readFile(
+        join(cliRoot, "templates/react-router-cloudflare/workers/app.ts"),
+        "utf8"
+      )
+    );
+  });
+
+  test("keeps webstudio-cloudflare-template function redirect handling synced with template", async () => {
+    await expect(
+      readFile(
+        join(
+          repoRoot,
+          "fixtures/webstudio-cloudflare-template/functions/[[path]].ts"
+        ),
+        "utf8"
+      )
+    ).resolves.toEqual(
+      await readFile(
+        join(cliRoot, "templates/cloudflare/functions/[[path]].ts"),
+        "utf8"
+      )
+    );
+  });
 });
 
 for (const {
diff --git a/packages/cli/templates/cloudflare/functions/[[path]].ts b/packages/cli/templates/cloudflare/functions/[[path]].ts
index 943b55594f13..d8de1b18d0d9 100644
--- a/packages/cli/templates/cloudflare/functions/[[path]].ts
+++ b/packages/cli/templates/cloudflare/functions/[[path]].ts
@@ -1,4 +1,9 @@
 import { createPagesFunctionHandler } from "@remix-run/cloudflare-pages";
+// @ts-ignore - app files are provided by the defaults template
+import { redirectRequest } from "../app/redirect-url";
+// @todo think about how to make __generated__ typeable
+// @ts-ignore
+import { redirects } from "../app/__generated__/$resources.redirects";
 
 // eslint-disable-next-line @typescript-eslint/ban-ts-comment
 // @ts-ignore - the server build file is generated by `remix vite:build`
@@ -6,4 +11,13 @@ import * as build from "../build/server";
 
 // eslint-disable-next-line @typescript-eslint/ban-ts-comment
 // @ts-ignore - the server build file is generated by `remix vite:build`
-export const onRequest = createPagesFunctionHandler({ build });
+const requestHandler = createPagesFunctionHandler({ build });
+
+export const onRequest: PagesFunction = (context) => {
+  const redirectResponse = redirectRequest(context.request, redirects);
+  if (redirectResponse !== undefined) {
+    return redirectResponse;
+  }
+
+  return requestHandler(context);
+};
diff --git a/packages/cli/templates/react-router-cloudflare/workers/app.ts b/packages/cli/templates/react-router-cloudflare/workers/app.ts
index 6d6f86672208..df05b6592566 100644
--- a/packages/cli/templates/react-router-cloudflare/workers/app.ts
+++ b/packages/cli/templates/react-router-cloudflare/workers/app.ts
@@ -1,4 +1,9 @@
 import { createRequestHandler } from "react-router";
+// @ts-ignore - app files are provided by the react-router template
+import { redirectRequest } from "../app/redirect-url";
+// @todo think about how to make __generated__ typeable
+// @ts-ignore
+import { redirects } from "../app/__generated__/$resources.redirects";
 
 declare module "react-router" {
   export interface AppLoadContext {
@@ -17,6 +22,11 @@ const requestHandler = createRequestHandler(
 
 export default {
   async fetch(request, env, ctx) {
+    const redirectResponse = redirectRequest(request, redirects);
+    if (redirectResponse !== undefined) {
+      return redirectResponse;
+    }
+
     return requestHandler(request, {
       EXCLUDE_FROM_SEARCH: false,
       getDefaultActionResource: undefined,