diff --git a/tests/conftest.py b/tests/conftest.py
index 587f2ef1..58dc5fb5 100644
--- a/tests/conftest.py
+++ b/tests/conftest.py
@@ -190,6 +190,32 @@ def _isolate_hermes_config_path():
     os.environ['HERMES_CONFIG_PATH'] = isolated_config_path
 
 
+@pytest.fixture(autouse=True)
+def _reset_password_hash_cache():
+    """Reset the memoized password-hash cache around every test (#5588).
+
+    api.auth.get_password_hash() caches the resolved hash process-wide
+    (_AUTH_HASH_CACHE / _AUTH_HASH_COMPUTED) for perf — it is NOT keyed on the
+    HERMES_WEBUI_PASSWORD env var. A test that sets that env var (e.g.
+    test_session_static_assets.test_session_static_auth_exemption) populates the
+    cache with a real hash; monkeypatch pops the env var on teardown but the
+    cache stays populated, so is_auth_enabled() reads stale True and later tests
+    (e.g. test_issue803's profile-cookie helpers) fail with a spurious
+    "requires a request handler when auth is enabled". Invalidate before AND
+    after each test so neither a pre-existing cached value nor a value this test
+    populates leaks across the isolation boundary. No-op when auth is off.
+    """
+    try:
+        from api.auth import _invalidate_password_hash_cache
+    except Exception:
+        _invalidate_password_hash_cache = None
+    if _invalidate_password_hash_cache:
+        _invalidate_password_hash_cache()
+    yield
+    if _invalidate_password_hash_cache:
+        _invalidate_password_hash_cache()
+
+
 _MISSING = object()  # sentinel: api.profiles module not loaded pre-test
 
 
diff --git a/tests/test_issue803.py b/tests/test_issue803.py
index 86835480..ff7bf8e9 100644
--- a/tests/test_issue803.py
+++ b/tests/test_issue803.py
@@ -34,6 +34,30 @@ class TestProfileCookieHelpers:
         assert 'SameSite=Lax' in s
         assert 'Path=/' in s
 
+    def test_build_profile_cookie_survives_stale_password_hash_cache(self, monkeypatch):
+        """#5588 regression: a prior test that set HERMES_WEBUI_PASSWORD populates
+        api.auth's process-wide password-hash cache; if that cache leaks past the
+        env-var teardown, is_auth_enabled() reads stale True and build_profile_cookie
+        raises "requires a request handler when auth is enabled". Simulate the leak
+        in-test: cache a password, pop the env, and confirm the memoized state does
+        not make a no-handler build_profile_cookie raise. (The autouse
+        _reset_password_hash_cache fixture is what keeps this from leaking across
+        real test files.)"""
+        import api.auth as auth
+        from api.helpers import build_profile_cookie
+        # Populate the cache as if an auth-enabled test just ran.
+        monkeypatch.setenv("HERMES_WEBUI_PASSWORD", "leak-check")
+        auth._invalidate_password_hash_cache()
+        assert auth.is_auth_enabled() is True  # cache now holds a hash
+        # Env goes away (as monkeypatch would on teardown) but reset the cache the
+        # way the autouse fixture does — auth must read as disabled again.
+        monkeypatch.delenv("HERMES_WEBUI_PASSWORD", raising=False)
+        auth._invalidate_password_hash_cache()
+        assert auth.is_auth_enabled() is False
+        # And the no-handler cookie build must not raise.
+        s = build_profile_cookie('alice')
+        assert 'hermes_profile=alice' in s
+
     def test_build_profile_cookie_default_persists(self):
         from api.helpers import build_profile_cookie
         s = build_profile_cookie('default')