diff --git a/src/gateway/server-tailscale.test.ts b/src/gateway/server-tailscale.test.ts
new file mode 100644
index 00000000000..fdc764f59af
--- /dev/null
+++ b/src/gateway/server-tailscale.test.ts
@@ -0,0 +1,107 @@
+import { beforeEach, describe, expect, it, vi } from "vitest";
+
+const tailscaleState = vi.hoisted(() => ({
+  enableServe: vi.fn(async (_port: number) => {}),
+  disableServe: vi.fn(async () => {}),
+  enableFunnel: vi.fn(async (_port: number) => {}),
+  disableFunnel: vi.fn(async () => {}),
+  getHost: vi.fn(async () => "gateway.tailnet.ts.net"),
+}));
+
+vi.mock("../infra/tailscale.js", () => ({
+  enableTailscaleServe: (port: number) => tailscaleState.enableServe(port),
+  disableTailscaleServe: () => tailscaleState.disableServe(),
+  enableTailscaleFunnel: (port: number) => tailscaleState.enableFunnel(port),
+  disableTailscaleFunnel: () => tailscaleState.disableFunnel(),
+  getTailnetHostname: () => tailscaleState.getHost(),
+}));
+
+import { startGatewayTailscaleExposure } from "./server-tailscale.js";
+
+function createOwnerStore() {
+  let currentToken: string | null = null;
+  let nextId = 0;
+
+  return {
+    async claim(mode: "serve" | "funnel", port: number) {
+      const record = {
+        token: `owner-${++nextId}`,
+        mode,
+        port,
+        pid: nextId,
+        claimedAt: new Date(0).toISOString(),
+      };
+      currentToken = record.token;
+      return record;
+    },
+    async isCurrentOwner(token: string) {
+      return currentToken === token;
+    },
+    async clearIfCurrentOwner(token: string) {
+      if (currentToken === token) {
+        currentToken = null;
+      }
+    },
+  };
+}
+
+describe("startGatewayTailscaleExposure", () => {
+  beforeEach(() => {
+    vi.clearAllMocks();
+  });
+
+  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,
+    });
+
+    await cleanupA?.();
+    expect(tailscaleState.disableServe).not.toHaveBeenCalled();
+    expect(logTailscale.info).toHaveBeenCalledWith(
+      "serve cleanup skipped: newer gateway owns Tailscale exposure",
+    );
+
+    await cleanupB?.();
+    expect(tailscaleState.disableServe).toHaveBeenCalledTimes(1);
+  });
+
+  it("clears ownership after a startup failure", async () => {
+    const ownerStore = createOwnerStore();
+    const logTailscale = {
+      info: vi.fn(),
+      warn: vi.fn(),
+    };
+    tailscaleState.enableServe.mockRejectedValueOnce(new Error("boom"));
+
+    const cleanup = await startGatewayTailscaleExposure({
+      tailscaleMode: "serve",
+      resetOnExit: true,
+      port: 18789,
+      logTailscale,
+      ownerStore,
+    });
+
+    expect(cleanup).not.toBeNull();
+    expect(logTailscale.warn).toHaveBeenCalledWith("serve failed: boom");
+
+    await cleanup?.();
+    expect(tailscaleState.disableServe).not.toHaveBeenCalled();
+  });
+});
diff --git a/src/gateway/server-tailscale.ts b/src/gateway/server-tailscale.ts
index 3dbdddb566c..74e394748d7 100644
--- a/src/gateway/server-tailscale.ts
+++ b/src/gateway/server-tailscale.ts
@@ -1,3 +1,7 @@
+import { randomUUID } from "node:crypto";
+import fs from "node:fs/promises";
+import path from "node:path";
+import { resolveGatewayLockDir } from "../config/paths.js";
 import {
   disableTailscaleFunnel,
   disableTailscaleServe,
@@ -6,17 +10,98 @@ import {
   getTailnetHostname,
 } from "../infra/tailscale.js";
 
+type GatewayTailscaleMode = "off" | "serve" | "funnel";
+
+type TailscaleExposureOwnerRecord = {
+  token: string;
+  mode: Exclude<GatewayTailscaleMode, "off">;
+  port: number;
+  pid: number;
+  claimedAt: string;
+};
+
+type TailscaleExposureOwnerStore = {
+  claim(
+    mode: Exclude<GatewayTailscaleMode, "off">,
+    port: number,
+  ): Promise<TailscaleExposureOwnerRecord>;
+  isCurrentOwner(token: string): Promise<boolean>;
+  clearIfCurrentOwner(token: string): Promise<void>;
+};
+
+function createTailscaleExposureOwnerStore(): TailscaleExposureOwnerStore {
+  const ownerFilePath = path.join(resolveGatewayLockDir(), "tailscale-exposure-owner.json");
+
+  async function readOwner(): Promise<TailscaleExposureOwnerRecord | null> {
+    try {
+      const raw = await fs.readFile(ownerFilePath, "utf8");
+      const parsed = JSON.parse(raw);
+      if (
+        parsed &&
+        typeof parsed === "object" &&
+        typeof parsed.token === "string" &&
+        typeof parsed.mode === "string" &&
+        typeof parsed.port === "number" &&
+        typeof parsed.pid === "number" &&
+        typeof parsed.claimedAt === "string"
+      ) {
+        return parsed as TailscaleExposureOwnerRecord;
+      }
+    } catch (err) {
+      if ((err as NodeJS.ErrnoException | undefined)?.code !== "ENOENT") {
+        // Ignore malformed or unreadable ownership state and continue.
+      }
+    }
+    return null;
+  }
+
+  return {
+    async claim(mode, port) {
+      const record: TailscaleExposureOwnerRecord = {
+        token: randomUUID(),
+        mode,
+        port,
+        pid: process.pid,
+        claimedAt: new Date().toISOString(),
+      };
+      await fs.mkdir(path.dirname(ownerFilePath), { recursive: true });
+      await fs.writeFile(ownerFilePath, JSON.stringify(record), "utf8");
+      return record;
+    },
+    async isCurrentOwner(token) {
+      const current = await readOwner();
+      return current?.token === token;
+    },
+    async clearIfCurrentOwner(token) {
+      if (!(await this.isCurrentOwner(token))) {
+        return;
+      }
+      try {
+        await fs.unlink(ownerFilePath);
+      } catch (err) {
+        if ((err as NodeJS.ErrnoException | undefined)?.code !== "ENOENT") {
+          throw err;
+        }
+      }
+    },
+  };
+}
+
 export async function startGatewayTailscaleExposure(params: {
-  tailscaleMode: "off" | "serve" | "funnel";
+  tailscaleMode: GatewayTailscaleMode;
   resetOnExit?: boolean;
   port: number;
   controlUiBasePath?: string;
   logTailscale: { info: (msg: string) => void; warn: (msg: string) => void };
+  ownerStore?: TailscaleExposureOwnerStore;
 }): Promise<(() => Promise<void>) | null> {
   if (params.tailscaleMode === "off") {
     return null;
   }
 
+  const ownerStore = params.ownerStore ?? createTailscaleExposureOwnerStore();
+  const owner = await ownerStore.claim(params.tailscaleMode, params.port);
+
   try {
     if (params.tailscaleMode === "serve") {
       await enableTailscaleServe(params.port);
@@ -33,6 +118,7 @@ export async function startGatewayTailscaleExposure(params: {
       params.logTailscale.info(`${params.tailscaleMode} enabled`);
     }
   } catch (err) {
+    await ownerStore.clearIfCurrentOwner(owner.token).catch(() => {});
     params.logTailscale.warn(
       `${params.tailscaleMode} failed: ${err instanceof Error ? err.message : String(err)}`,
     );
@@ -44,11 +130,18 @@ export async function startGatewayTailscaleExposure(params: {
 
   return async () => {
     try {
+      if (!(await ownerStore.isCurrentOwner(owner.token))) {
+        params.logTailscale.info(
+          `${params.tailscaleMode} cleanup skipped: newer gateway owns Tailscale exposure`,
+        );
+        return;
+      }
       if (params.tailscaleMode === "serve") {
         await disableTailscaleServe();
       } else {
         await disableTailscaleFunnel();
       }
+      await ownerStore.clearIfCurrentOwner(owner.token);
     } catch (err) {
       params.logTailscale.warn(
         `${params.tailscaleMode} cleanup failed: ${err instanceof Error ? err.message : String(err)}`,