diff --git a/src/gateway/server-tailscale.test.ts b/src/gateway/server-tailscale.test.ts
index 75fe443dea2..29575d6f743 100644
--- a/src/gateway/server-tailscale.test.ts
+++ b/src/gateway/server-tailscale.test.ts
@@ -59,74 +59,141 @@ function createOwnerStore() {
   };
 }
 
-describe("startGatewayTailscaleExposure", () => {
-  beforeEach(() => {
-    vi.clearAllMocks();
-  });
+const modeCases = [
+  {
+    mode: "serve" as const,
+    enableMock: tailscaleState.enableServe,
+    disableMock: tailscaleState.disableServe,
+  },
+  {
+    mode: "funnel" as const,
+    enableMock: tailscaleState.enableFunnel,
+    disableMock: tailscaleState.disableFunnel,
+  },
+];
 
-  it("skips stale serve cleanup after a newer gateway takes ownership", async () => {
-    const ownerStore = createOwnerStore();
-    const logTailscale = {
-      info: vi.fn(),
-      warn: vi.fn(),
-    };
-
-    const cleanupA = await startGatewayTailscaleExposure({
-      tailscaleMode: "serve",
-      resetOnExit: true,
-      port: 18789,
-      logTailscale,
-      ownerStore,
-    });
-    const cleanupB = await startGatewayTailscaleExposure({
-      tailscaleMode: "serve",
-      resetOnExit: true,
-      port: 18789,
-      logTailscale,
-      ownerStore,
+describe.each(modeCases)(
+  "startGatewayTailscaleExposure (%s)",
+  ({ mode, enableMock, disableMock }) => {
+    beforeEach(() => {
+      vi.restoreAllMocks();
+      vi.clearAllMocks();
     });
 
-    await cleanupA?.();
-    expect(tailscaleState.disableServe).not.toHaveBeenCalled();
-    expect(logTailscale.info).toHaveBeenCalledWith("serve cleanup skipped: not the current owner");
+    it("skips stale cleanup after a newer gateway takes ownership", async () => {
+      const ownerStore = createOwnerStore();
+      const logTailscale = {
+        info: vi.fn(),
+        warn: vi.fn(),
+      };
 
-    await cleanupB?.();
-    expect(tailscaleState.disableServe).toHaveBeenCalledTimes(1);
-  });
+      const cleanupA = await startGatewayTailscaleExposure({
+        tailscaleMode: mode,
+        resetOnExit: true,
+        port: 18789,
+        logTailscale,
+        ownerStore,
+      });
+      const cleanupB = await startGatewayTailscaleExposure({
+        tailscaleMode: mode,
+        resetOnExit: true,
+        port: 18789,
+        logTailscale,
+        ownerStore,
+      });
 
-  it("restores the previous owner after a takeover startup failure", async () => {
-    const ownerStore = createOwnerStore();
-    const logTailscale = {
-      info: vi.fn(),
-      warn: vi.fn(),
-    };
+      await cleanupA?.();
+      expect(disableMock).not.toHaveBeenCalled();
+      expect(logTailscale.info).toHaveBeenCalledWith(
+        `${mode} cleanup skipped: not the current owner`,
+      );
 
-    const cleanupA = await startGatewayTailscaleExposure({
-      tailscaleMode: "serve",
-      resetOnExit: true,
-      port: 18789,
-      logTailscale,
-      ownerStore,
+      await cleanupB?.();
+      expect(disableMock).toHaveBeenCalledTimes(1);
     });
 
-    tailscaleState.enableServe.mockRejectedValueOnce(new Error("boom"));
+    it("restores the previous live owner after a takeover startup failure", async () => {
+      const ownerStore = createOwnerStore();
+      const logTailscale = {
+        info: vi.fn(),
+        warn: vi.fn(),
+      };
 
-    const cleanupB = await startGatewayTailscaleExposure({
-      tailscaleMode: "serve",
-      resetOnExit: true,
-      port: 18789,
-      logTailscale,
-      ownerStore,
+      const cleanupA = await startGatewayTailscaleExposure({
+        tailscaleMode: mode,
+        resetOnExit: true,
+        port: 18789,
+        logTailscale,
+        ownerStore,
+      });
+
+      enableMock.mockRejectedValueOnce(new Error("boom"));
+
+      const cleanupB = await startGatewayTailscaleExposure({
+        tailscaleMode: mode,
+        resetOnExit: true,
+        port: 18789,
+        logTailscale,
+        ownerStore,
+      });
+
+      expect(cleanupB).not.toBeNull();
+      expect(logTailscale.warn).toHaveBeenCalledWith(`${mode} failed: boom`);
+
+      await cleanupB?.();
+      expect(disableMock).not.toHaveBeenCalled();
+      expect(logTailscale.info).toHaveBeenCalledWith(
+        `${mode} cleanup skipped: not the current owner`,
+      );
+
+      await cleanupA?.();
+      expect(disableMock).toHaveBeenCalledTimes(1);
     });
 
-    expect(cleanupB).not.toBeNull();
-    expect(logTailscale.warn).toHaveBeenCalledWith("serve failed: boom");
+    it("keeps the failed owner when the previous owner is already gone", async () => {
+      const ownerStore = createOwnerStore();
+      const logTailscale = {
+        info: vi.fn(),
+        warn: vi.fn(),
+      };
 
-    await cleanupB?.();
-    expect(tailscaleState.disableServe).not.toHaveBeenCalled();
-    expect(logTailscale.info).toHaveBeenCalledWith("serve cleanup skipped: not the current owner");
+      const cleanupA = await startGatewayTailscaleExposure({
+        tailscaleMode: mode,
+        resetOnExit: true,
+        port: 18789,
+        logTailscale,
+        ownerStore,
+      });
 
-    await cleanupA?.();
-    expect(tailscaleState.disableServe).toHaveBeenCalledTimes(1);
-  });
-});
+      vi.spyOn(process, "kill").mockImplementation(((pid: number) => {
+        if (pid === 1) {
+          const err = new Error("gone") as NodeJS.ErrnoException;
+          err.code = "ESRCH";
+          throw err;
+        }
+        return true;
+      }) as typeof process.kill);
+      enableMock.mockRejectedValueOnce(new Error("boom"));
+
+      const cleanupB = await startGatewayTailscaleExposure({
+        tailscaleMode: mode,
+        resetOnExit: true,
+        port: 18789,
+        logTailscale,
+        ownerStore,
+      });
+
+      expect(cleanupB).not.toBeNull();
+      expect(logTailscale.warn).toHaveBeenCalledWith(`${mode} failed: boom`);
+
+      await cleanupA?.();
+      expect(disableMock).not.toHaveBeenCalled();
+      expect(logTailscale.info).toHaveBeenCalledWith(
+        `${mode} cleanup skipped: not the current owner`,
+      );
+
+      await cleanupB?.();
+      expect(disableMock).toHaveBeenCalledTimes(1);
+    });
+  },
+);
diff --git a/src/gateway/server-tailscale.ts b/src/gateway/server-tailscale.ts
index 9bc18d1e660..73dfb792fae 100644
--- a/src/gateway/server-tailscale.ts
+++ b/src/gateway/server-tailscale.ts
@@ -32,6 +32,15 @@ type TailscaleExposureOwnerStore = {
   runCleanupIfCurrentOwner(token: string, cleanup: () => Promise<void>): Promise<boolean>;
 };
 
+function isPidAlive(pid: number): boolean {
+  try {
+    process.kill(pid, 0);
+    return true;
+  } catch (err) {
+    return (err as NodeJS.ErrnoException | undefined)?.code !== "ESRCH";
+  }
+}
+
 function createTailscaleExposureOwnerStore(): TailscaleExposureOwnerStore {
   const ownerFilePath = path.join(resolveGatewayLockDir(), "tailscale-exposure-owner.json");
   const ownerLockPath = path.join(resolveGatewayLockDir(), "tailscale-exposure-owner.lock");
@@ -64,29 +73,15 @@ function createTailscaleExposureOwnerStore(): TailscaleExposureOwnerStore {
     await new Promise((resolve) => setTimeout(resolve, ms));
   }
 
-  function isPidAlive(pid: number): boolean {
-    try {
-      process.kill(pid, 0);
-      return true;
-    } catch (err) {
-      return (err as NodeJS.ErrnoException | undefined)?.code !== "ESRCH";
-    }
-  }
-
   async function breakStaleLock() {
     try {
-      const [raw, stat] = await Promise.all([
-        fs.readFile(ownerLockPath, "utf8").catch(() => null),
-        fs.stat(ownerLockPath),
-      ]);
+      const stat = await fs.stat(ownerLockPath);
       if (Date.now() - stat.mtimeMs < lockStaleMs) {
         return;
       }
-      const parsed = raw ? JSON.parse(raw) : null;
-      const pid = typeof parsed?.pid === "number" ? parsed.pid : null;
-      if (pid !== null && isPidAlive(pid)) {
-        return;
-      }
+      // All lock holders only perform short file I/O plus the Tailscale CLI calls,
+      // and those helpers already time out after 15s. If the lock still exists after
+      // the wider stale window, assume the holder is wedged and break it.
       await fs.unlink(ownerLockPath).catch(() => {});
     } catch (err) {
       if ((err as NodeJS.ErrnoException | undefined)?.code !== "ENOENT") {
@@ -202,7 +197,13 @@ export async function startGatewayTailscaleExposure(params: {
       params.logTailscale.info(`${params.tailscaleMode} enabled`);
     }
   } catch (err) {
-    await ownerStore.replaceIfCurrent(owner.token, previousOwner).catch(() => {});
+    const nextOwner =
+      previousOwner && isPidAlive(previousOwner.pid)
+        ? previousOwner
+        : params.resetOnExit
+          ? owner
+          : null;
+    await ownerStore.replaceIfCurrent(owner.token, nextOwner).catch(() => {});
     params.logTailscale.warn(
       `${params.tailscaleMode} failed: ${err instanceof Error ? err.message : String(err)}`,
     );