diff --git a/apps/cloud/src/edge/index.ts b/apps/cloud/src/edge/index.ts
index bdb166892..1b1cbe9ad 100644
--- a/apps/cloud/src/edge/index.ts
+++ b/apps/cloud/src/edge/index.ts
@@ -9,3 +9,4 @@ export { marketingMiddleware } from "./marketing";
 export { sentryTunnelMiddleware } from "./sentry-tunnel";
 export { posthogProxyMiddleware } from "./posthog";
 export { docsProxyMiddleware } from "./docs";
+export { openAiAppsChallengeMiddleware } from "./openai-apps-challenge";
diff --git a/apps/cloud/src/edge/openai-apps-challenge.test.ts b/apps/cloud/src/edge/openai-apps-challenge.test.ts
new file mode 100644
index 000000000..26fa95e65
--- /dev/null
+++ b/apps/cloud/src/edge/openai-apps-challenge.test.ts
@@ -0,0 +1,29 @@
+import { describe, expect, it } from "@effect/vitest";
+
+import {
+  OPENAI_APPS_CHALLENGE_PATH,
+  OPENAI_APPS_CHALLENGE_TOKEN,
+  isOpenAiAppsChallengePath,
+  openAiAppsChallengeResponse,
+} from "./openai-apps-challenge";
+
+describe("isOpenAiAppsChallengePath", () => {
+  it("claims the OpenAI Apps verification challenge path", () => {
+    expect(isOpenAiAppsChallengePath(OPENAI_APPS_CHALLENGE_PATH)).toBe(true);
+  });
+
+  it("does not claim sibling well-known paths", () => {
+    expect(isOpenAiAppsChallengePath("/.well-known/openai-apps-challenge/extra")).toBe(false);
+    expect(isOpenAiAppsChallengePath("/.well-known/oauth-protected-resource/mcp")).toBe(false);
+  });
+});
+
+describe("openAiAppsChallengeResponse", () => {
+  it("serves the exact verification token as plain text", async () => {
+    const response = openAiAppsChallengeResponse();
+
+    expect(response.status).toBe(200);
+    expect(response.headers.get("content-type")).toBe("text/plain; charset=utf-8");
+    expect(await response.text()).toBe(OPENAI_APPS_CHALLENGE_TOKEN);
+  });
+});
diff --git a/apps/cloud/src/edge/openai-apps-challenge.ts b/apps/cloud/src/edge/openai-apps-challenge.ts
new file mode 100644
index 000000000..a3ba1fff0
--- /dev/null
+++ b/apps/cloud/src/edge/openai-apps-challenge.ts
@@ -0,0 +1,23 @@
+import { createMiddleware } from "@tanstack/react-start";
+
+export const OPENAI_APPS_CHALLENGE_PATH = "/.well-known/openai-apps-challenge";
+export const OPENAI_APPS_CHALLENGE_TOKEN =
+  "P_fW7WgF8HkXXQkP85B7aDZD_RuZv8YmQA2Zq9JoIfc";
+
+export const isOpenAiAppsChallengePath = (pathname: string) =>
+  pathname === OPENAI_APPS_CHALLENGE_PATH;
+
+export const openAiAppsChallengeResponse = () =>
+  new Response(OPENAI_APPS_CHALLENGE_TOKEN, {
+    headers: {
+      "cache-control": "public, max-age=300",
+      "content-type": "text/plain; charset=utf-8",
+    },
+  });
+
+export const openAiAppsChallengeMiddleware = createMiddleware({ type: "request" }).server(
+  ({ pathname, next }) => {
+    if (!isOpenAiAppsChallengePath(pathname)) return next();
+    return openAiAppsChallengeResponse();
+  },
+);
diff --git a/apps/cloud/src/start.ts b/apps/cloud/src/start.ts
index d0e92dd3b..a35a327f1 100644
--- a/apps/cloud/src/start.ts
+++ b/apps/cloud/src/start.ts
@@ -11,6 +11,7 @@ import { prepareMcpOrgScope } from "./mcp/mount";
 import {
   docsProxyMiddleware,
   marketingMiddleware,
+  openAiAppsChallengeMiddleware,
   posthogProxyMiddleware,
   sentryTunnelMiddleware,
 } from "./edge";
@@ -100,6 +101,7 @@ const appRequestMiddleware = createMiddleware({ type: "request" }).server(
 // load-bearing.
 export const startInstance = createStart(() => ({
   requestMiddleware: [
+    openAiAppsChallengeMiddleware,
     marketingMiddleware,
     docsProxyMiddleware,
     sentryTunnelMiddleware,