diff --git a/app/api/auth/impersonate/route.ts b/app/api/auth/impersonate/route.ts
index bef1b35f4..6690be6ff 100644
--- a/app/api/auth/impersonate/route.ts
+++ b/app/api/auth/impersonate/route.ts
@@ -7,11 +7,8 @@ import { getCookieOptions } from '@/lib/oauth/cookie-config';
 import { normalizeJmapServerUrl } from '@/lib/auth/verify-jmap-auth';
 import { setStalwartAuthContextInStore } from '@/lib/stalwart/auth-context';
 import { recordLogin } from '@/lib/telemetry/login-tracker';
-import {
-  ImpersonationJwtError,
-  impersonationReplayCache,
-  verifyImpersonationJwt,
-} from '@/lib/impersonation/jwt';
+import { ImpersonationJwtError, verifyImpersonationJwt } from '@/lib/impersonation/jwt';
+import { consumeImpersonationJti } from '@/lib/impersonation/replay-store';
 import {
   readImpersonationConfig,
   resolveImpersonationServerUrl,
@@ -81,7 +78,7 @@ export async function GET(request: NextRequest) {
     return NextResponse.json({ error: 'Internal server error' }, { status: 500 });
   }
 
-  if (!impersonationReplayCache.consume(claims.jti, claims.exp)) {
+  if (!(await consumeImpersonationJti(claims.jti, claims.exp))) {
     logger.warn('Impersonation JWT replay rejected', { jti: claims.jti });
     return NextResponse.json({ error: 'Token already used' }, { status: 401 });
   }
diff --git a/lib/__tests__/impersonation-replay-store.test.ts b/lib/__tests__/impersonation-replay-store.test.ts
new file mode 100644
index 000000000..b1e3464d6
--- /dev/null
+++ b/lib/__tests__/impersonation-replay-store.test.ts
@@ -0,0 +1,58 @@
+// @vitest-environment node
+import { mkdtempSync, readdirSync, rmSync, utimesSync } from 'node:fs';
+import { tmpdir } from 'node:os';
+import path from 'node:path';
+import { afterEach, beforeEach, describe, expect, it, vi } from 'vitest';
+
+vi.mock('@/lib/logger', () => ({
+  logger: { warn: vi.fn(), info: vi.fn(), error: vi.fn(), debug: vi.fn() },
+}));
+
+import { IMPERSONATION_REPLAY_WINDOW_SEC, impersonationReplayCache } from '@/lib/impersonation/jwt';
+import { consumeImpersonationJti } from '@/lib/impersonation/replay-store';
+
+// The jti cache lived only in process memory: after a restart, or on another
+// replica, a captured handoff link could be redeemed again.
+
+let stateDir: string;
+const previous = process.env.ADMIN_STATE_DIR;
+
+beforeEach(() => {
+  stateDir = mkdtempSync(path.join(tmpdir(), 'bw-jti-'));
+  process.env.ADMIN_STATE_DIR = stateDir;
+  impersonationReplayCache.clear();
+});
+
+afterEach(() => {
+  if (previous === undefined) delete process.env.ADMIN_STATE_DIR;
+  else process.env.ADMIN_STATE_DIR = previous;
+  rmSync(stateDir, { recursive: true, force: true });
+});
+
+describe('consumeImpersonationJti', () => {
+  const now = Date.now();
+  const exp = Math.floor(now / 1000) + 120;
+
+  it('refuses a jti the second time', async () => {
+    expect(await consumeImpersonationJti('jti-1', exp, now)).toBe(true);
+    expect(await consumeImpersonationJti('jti-1', exp, now)).toBe(false);
+  });
+
+  it('still refuses it after the in-process cache is gone (restart, other replica)', async () => {
+    expect(await consumeImpersonationJti('jti-1', exp, now)).toBe(true);
+    impersonationReplayCache.clear();
+    expect(await consumeImpersonationJti('jti-1', exp, now)).toBe(false);
+  });
+
+  it('prunes markers once their token can no longer verify', async () => {
+    await consumeImpersonationJti('jti-old', exp, now);
+    const dir = path.join(stateDir, 'impersonation-jti');
+    const [marker] = readdirSync(dir);
+    const old = (now - (IMPERSONATION_REPLAY_WINDOW_SEC + 5) * 1000) / 1000;
+    utimesSync(path.join(dir, marker), old, old);
+
+    await consumeImpersonationJti('jti-new', exp, now);
+    expect(readdirSync(dir)).toHaveLength(1);
+    expect(readdirSync(dir)).not.toContain(marker);
+  });
+});
diff --git a/lib/__tests__/impersonation-session.test.ts b/lib/__tests__/impersonation-session.test.ts
index 1920f148d..8202b5aff 100644
--- a/lib/__tests__/impersonation-session.test.ts
+++ b/lib/__tests__/impersonation-session.test.ts
@@ -1,6 +1,9 @@
 // @vitest-environment node
 import { createHmac, randomUUID } from 'node:crypto';
-import { afterEach, beforeAll, beforeEach, describe, expect, it, vi } from 'vitest';
+import { mkdtempSync, rmSync } from 'node:fs';
+import { tmpdir } from 'node:os';
+import path from 'node:path';
+import { afterAll, afterEach, beforeAll, beforeEach, describe, expect, it, vi } from 'vitest';
 import { NextRequest } from 'next/server';
 
 vi.mock('@/lib/auth/session-secret', () => ({
@@ -78,7 +81,12 @@ async function readSession() {
 }
 
 describe('impersonation handoff', () => {
+  // Used jtis are recorded in the state directory.
+  const stateDir = mkdtempSync(path.join(tmpdir(), 'bw-imp-'));
+  afterAll(() => rmSync(stateDir, { recursive: true, force: true }));
+
   beforeAll(() => {
+    process.env.ADMIN_STATE_DIR = stateDir;
     process.env.BULWARK_JWT_AUTH_SECRET = SECRET;
     process.env.BULWARK_STALWART_MASTER_USER = 'master@example.org';
     process.env.BULWARK_STALWART_MASTER_PASSWORD = MASTER_PASSWORD;
diff --git a/lib/impersonation/jwt.ts b/lib/impersonation/jwt.ts
index 4145ce138..d7d3edeff 100644
--- a/lib/impersonation/jwt.ts
+++ b/lib/impersonation/jwt.ts
@@ -26,6 +26,13 @@ const MAX_TOKEN_LIFETIME_SEC = 300;
 const CLOCK_SKEW_SEC = 60;
 const MIN_SECRET_LENGTH = 32;
 
+/**
+ * How long after it is first redeemed a token can still verify: `iat` may
+ * run CLOCK_SKEW_SEC ahead, `exp` is at most MAX_TOKEN_LIFETIME_SEC after
+ * `iat`, and `exp` is honoured for another CLOCK_SKEW_SEC.
+ */
+export const IMPERSONATION_REPLAY_WINDOW_SEC = MAX_TOKEN_LIFETIME_SEC + 2 * CLOCK_SKEW_SEC;
+
 function base64UrlDecode(input: string): Buffer {
   const pad = input.length % 4 === 0 ? 0 : 4 - (input.length % 4);
   const b64 = input.replace(/-/g, '+').replace(/_/g, '/') + '='.repeat(pad);
@@ -141,12 +148,10 @@ export function verifyImpersonationJwt(
 
 // ─── Replay protection ──────────────────────────────────────────
 // In-memory LRU keyed by jti. Entries expire automatically once their
-// underlying JWT could no longer be replayed (exp + skew). On a multi-pod
-// deployment each pod has its own cache; that's acceptable because a token
-// stolen mid-flight could only be replayed against the pod that already
-// consumed it (and that pod will reject it). For stronger guarantees,
-// platforms can issue per-pod-routed tokens or front Bulwark with a
-// single-leader load balancer for the impersonate route.
+// underlying JWT could no longer be replayed (exp + skew). This is the fast
+// path; consumeImpersonationJti() in replay-store.ts backs it with marker
+// files in the state directory so a restart or another replica sharing the
+// state volume still refuses a used token.
 
 const REPLAY_CACHE_MAX = 4096;
 
diff --git a/lib/impersonation/replay-store.ts b/lib/impersonation/replay-store.ts
new file mode 100644
index 000000000..6f3cba8ac
--- /dev/null
+++ b/lib/impersonation/replay-store.ts
@@ -0,0 +1,55 @@
+import { createHash } from 'node:crypto';
+import { mkdir, open, readdir, stat, unlink } from 'node:fs/promises';
+import path from 'node:path';
+import { getStatePath } from '@/lib/admin/paths';
+import { logger } from '@/lib/logger';
+import { IMPERSONATION_REPLAY_WINDOW_SEC, impersonationReplayCache } from './jwt';
+
+const STORE_DIR = 'impersonation-jti';
+
+async function pruneExpired(dir: string, nowMs: number): Promise<void> {
+  for (const name of await readdir(dir)) {
+    const file = path.join(dir, name);
+    try {
+      const { mtimeMs } = await stat(file);
+      if (nowMs - mtimeMs > IMPERSONATION_REPLAY_WINDOW_SEC * 1000) await unlink(file);
+    } catch {
+      // Another process pruned it first.
+    }
+  }
+}
+
+/**
+ * Record an impersonation token's jti as used; false when it was used before.
+ *
+ * The in-process cache alone forgot every jti on restart and knew nothing of
+ * other replicas, so a captured handoff link could be redeemed again within
+ * its lifetime. Each jti also gets a marker file in the state directory,
+ * created with O_EXCL, which survives restarts and is shared by every
+ * replica that mounts the same state volume. Markers are pruned once the
+ * token they stand for can no longer verify.
+ */
+export async function consumeImpersonationJti(
+  jti: string,
+  exp: number,
+  nowMs: number = Date.now(),
+): Promise<boolean> {
+  if (!impersonationReplayCache.consume(jti, exp, Math.floor(nowMs / 1000))) return false;
+
+  const dir = getStatePath(STORE_DIR);
+  try {
+    await mkdir(dir, { recursive: true });
+    await pruneExpired(dir, nowMs);
+    const marker = await open(path.join(dir, createHash('sha256').update(jti).digest('hex')), 'wx');
+    await marker.close();
+    return true;
+  } catch (err) {
+    if ((err as NodeJS.ErrnoException).code === 'EEXIST') return false;
+    // The state directory is documented as always writable; if it is not,
+    // keep impersonation working on the in-process cache.
+    logger.warn('Impersonation replay store unavailable, using the in-process cache only', {
+      error: err instanceof Error ? err.message : 'Unknown',
+    });
+    return true;
+  }
+}