diff --git a/app.py b/app.py
index bb4f51ffb..80eb83c85 100644
--- a/app.py
+++ b/app.py
@@ -313,6 +313,7 @@ if AUTH_ENABLED:
 
     def _refresh_token_cache():
         """Rebuild the prefix→[(id,hash)] map from the DB."""
+        global _token_cache
         from collections import defaultdict
         new_map = defaultdict(list)
         db = SessionLocal()
@@ -331,8 +332,8 @@ if AUTH_ENABLED:
                 new_map[r.token_prefix].append((r.id, r.token_hash, owner_key, scopes))
         finally:
             db.close()
-        _token_cache.clear()
-        _token_cache.update(new_map)
+        _token_cache = dict(new_map)
+        app.state._token_cache = _token_cache
         app.state._token_cache_dirty = False
 
     # Headers that prove a request was forwarded by a proxy/tunnel (cloudflared,
diff --git a/tests/test_token_cache_atomic_swap.py b/tests/test_token_cache_atomic_swap.py
new file mode 100644
index 000000000..f32f93097
--- /dev/null
+++ b/tests/test_token_cache_atomic_swap.py
@@ -0,0 +1,188 @@
+"""Regression test for token cache race condition.
+
+Exercises the actual _refresh_token_cache() and _token_cache in app.py
+to verify the atomic swap fix eliminates the race window.
+"""
+import os
+import sys
+import threading
+import time
+from types import SimpleNamespace
+from unittest.mock import MagicMock
+
+import pytest
+
+
+@pytest.fixture
+def app_module(monkeypatch):
+    """Import app.py with AUTH_ENABLED=true and minimal mocked deps.
+
+    Sets up a real AuthManager user ('admin') so normalize_known_username
+    resolves the token owner.  Replaces SessionLocal with a MagicMock so
+    _refresh_token_cache() can run without a real DB.
+    """
+    monkeypatch.setenv("AUTH_ENABLED", "true")
+    monkeypatch.setenv("DATABASE_URL", "sqlite:///:memory:")
+
+    # Clear cached app module
+    monkeypatch.delitem(sys.modules, "app", raising=False)
+
+    import app as app_mod  # noqa: E402
+
+    app_mod.SessionLocal = MagicMock()
+    app_mod.logger = MagicMock()
+    app_mod.auth_manager.setup("admin", "TestPass123!")
+
+    return app_mod
+
+
+def _seed(app_mod, rows):
+    """Set up the mocked SessionLocal to return *rows* on next query."""
+    app_mod.SessionLocal.return_value.query.return_value.filter.return_value.all.return_value = rows
+
+
+def _row(prefix, tid="t1", th="h1", owner="admin", scopes="chat"):
+    return SimpleNamespace(
+        token_prefix=prefix, id=tid, token_hash=th,
+        owner=owner, scopes=scopes, is_active=True,
+    )
+
+
+# ---------------------------------------------------------------------------
+# Tests — all use the REAL app._refresh_token_cache and REAL app._token_cache
+# ---------------------------------------------------------------------------
+
+class TestRefreshPopulatesCache:
+    """Single refresh call should populate _token_cache from DB rows."""
+
+    def test_single_row(self, app_module):
+        _seed(app_module, [_row("ody_abc")])
+        app_module.app.state._token_cache_dirty = True
+        app_module._refresh_token_cache()
+        assert "ody_abc" in app_module._token_cache
+        assert app_module._token_cache["ody_abc"][0][0] == "t1"
+
+    def test_multiple_prefixes(self, app_module):
+        _seed(app_module, [
+            _row("ody_aaaa", "t1", "h1", "admin", "chat"),
+            _row("ody_bbbb", "t2", "h2", "admin", "chat,tools"),
+            _row("ody_aaaa", "t3", "h3", "admin", "memory"),
+        ])
+        app_module.app.state._token_cache_dirty = True
+        app_module._refresh_token_cache()
+        assert len(app_module._token_cache) == 2
+        assert len(app_module._token_cache["ody_aaaa"]) == 2
+        assert app_module._token_cache["ody_bbbb"][0][3] == ["chat", "tools"]
+
+    def test_empty_db_clears_cache(self, app_module):
+        app_module._token_cache["stale"] = [("x", "y", "z", ["chat"])]
+        _seed(app_module, [])
+        app_module.app.state._token_cache_dirty = True
+        app_module._refresh_token_cache()
+        assert len(app_module._token_cache) == 0
+
+
+class TestAppStateSync:
+    """app.state._token_cache must stay synchronized with _token_cache."""
+
+    def test_state_ref_matches_after_refresh(self, app_module):
+        _seed(app_module, [_row("ody_sync")])
+        app_module.app.state._token_cache_dirty = True
+        app_module._refresh_token_cache()
+        assert app_module.app.state._token_cache is app_module._token_cache
+        assert "ody_sync" in app_module.app.state._token_cache
+
+    def test_state_dirty_cleared(self, app_module):
+        _seed(app_module, [_row("ody_x")])
+        app_module.app.state._token_cache_dirty = True
+        app_module._refresh_token_cache()
+        assert app_module.app.state._token_cache_dirty is False
+
+
+class TestConcurrentReaders:
+    """The core regression: concurrent readers must never see an empty cache."""
+
+    def test_no_empty_reads_during_refresh(self, app_module):
+        """4 reader threads + 100 refreshes on the real _token_cache global."""
+        _seed(app_module, [_row("ody_race")])
+        app_module.app.state._token_cache_dirty = True
+        app_module._refresh_token_cache()
+
+        stop = threading.Event()
+        results = {"empty": 0, "ok": 0}
+
+        def reader():
+            while not stop.is_set():
+                if len(app_module._token_cache) == 0:
+                    results["empty"] += 1
+                else:
+                    results["ok"] += 1
+
+        def churner():
+            for _ in range(100):
+                app_module._refresh_token_cache()
+
+        readers = [threading.Thread(target=reader, daemon=True) for _ in range(4)]
+        for t in readers:
+            t.start()
+
+        churn = threading.Thread(target=churner)
+        churn.start()
+
+        time.sleep(0.1)
+        churn.join(timeout=5)
+        stop.set()
+        for t in readers:
+            t.join(timeout=2)
+
+        assert results["empty"] == 0, (
+            "Readers saw empty cache %d times (ok=%d)"
+            % (results["empty"], results["ok"])
+        )
+        assert results["ok"] > 0
+
+    def test_no_empty_reads_with_token_churn(self, app_module):
+        """Simulate token create/revoke churn while reading."""
+        _seed(app_module, [_row("ody_keep", "t1", "h1", "admin", "chat")])
+        app_module.app.state._token_cache_dirty = True
+        app_module._refresh_token_cache()
+
+        stop = threading.Event()
+        results = {"empty": 0, "ok": 0}
+
+        def reader():
+            while not stop.is_set():
+                if len(app_module._token_cache) == 0:
+                    results["empty"] += 1
+                else:
+                    results["ok"] += 1
+
+        def churner():
+            for i in range(50):
+                _seed(app_module, [
+                    _row("ody_keep", "t1", "h1", "admin", "chat"),
+                    _row("ody_new_%d" % i, "t%d" % (i + 10), "h%d" % (i + 10), "admin", "chat"),
+                ])
+                app_module._refresh_token_cache()
+                _seed(app_module, [_row("ody_keep", "t1", "h1", "admin", "chat")])
+                app_module._refresh_token_cache()
+
+        readers = [threading.Thread(target=reader, daemon=True) for _ in range(4)]
+        for t in readers:
+            t.start()
+
+        churn = threading.Thread(target=churner)
+        churn.start()
+
+        churn.join(timeout=10)
+        stop.set()
+        for t in readers:
+            t.join(timeout=2)
+
+        assert results["empty"] == 0, (
+            "Readers saw empty cache %d times during churn (ok=%d)"
+            % (results["empty"], results["ok"])
+        )
+        assert results["ok"] > 0
+        assert "ody_keep" in app_module._token_cache
+        assert len(app_module._token_cache) == 1