diff --git a/hermes_cli/web_server.py b/hermes_cli/web_server.py
index 08d0ac32bda..061a2e46816 100644
--- a/hermes_cli/web_server.py
+++ b/hermes_cli/web_server.py
@@ -246,7 +246,31 @@ def _has_valid_session_token(request: Request) -> bool:
 
 
 def _require_token(request: Request) -> None:
-    """Validate the ephemeral session token.  Raises 401 on mismatch."""
+    """Authorize a sensitive endpoint, raising 401 if the caller isn't allowed.
+
+    Two auth schemes protect the dashboard, exactly one active per bind:
+
+    * **Loopback / ``--insecure`` mode** (``auth_required`` False): the
+      ephemeral ``_SESSION_TOKEN`` is injected into the SPA HTML and echoed
+      back via ``X-Hermes-Session-Token`` (or the legacy ``Bearer`` header).
+      Validate it here.
+    * **Gated / OAuth mode** (``auth_required`` True): ``_SESSION_TOKEN`` is
+      NOT injected (the SPA authenticates with a session cookie), so there is
+      no token to check. The ``gated_auth_middleware`` has already verified the
+      cookie before the request reached this handler — any non-public ``/api/``
+      route it lets through carries a verified ``request.state.session``. The
+      legacy ``auth_middleware`` likewise short-circuits in this mode. Requiring
+      the (absent) token here would 401 every cookie-authenticated request,
+      making plugin install/enable/disable and the other ``_require_token``
+      endpoints permanently unreachable behind the gate. Defer to the gate.
+    """
+    if getattr(request.app.state, "auth_required", False):
+        # Gate is authoritative. It attaches ``request.state.session`` on
+        # success and 401s otherwise, so a request that reached us is already
+        # authenticated. Belt-and-braces: confirm the session is present.
+        if getattr(request.state, "session", None) is not None:
+            return
+        raise HTTPException(status_code=401, detail="Unauthorized")
     if not _has_valid_session_token(request):
         raise HTTPException(status_code=401, detail="Unauthorized")
 
diff --git a/tests/hermes_cli/test_dashboard_auth_middleware.py b/tests/hermes_cli/test_dashboard_auth_middleware.py
index a7363a1db8a..2e1abd4cdf1 100644
--- a/tests/hermes_cli/test_dashboard_auth_middleware.py
+++ b/tests/hermes_cli/test_dashboard_auth_middleware.py
@@ -191,6 +191,111 @@ def test_full_login_round_trip_unlocks_gated_api(gated_app):
     )
 
 
+def _complete_stub_login(client) -> None:
+    """Walk the stub OAuth round trip so ``client`` carries a valid session.
+
+    TestClient persists Set-Cookie across calls, so after this returns the
+    client's cookie jar holds ``hermes_session_at`` / ``hermes_session_rt``
+    and subsequent gated requests authenticate.
+    """
+    r1 = client.get("/auth/login?provider=stub", follow_redirects=False)
+    assert r1.status_code == 302
+    state = r1.headers["location"].split("state=")[1]
+    r2 = client.get(
+        f"/auth/callback?code=stub_code&state={state}",
+        follow_redirects=False,
+    )
+    assert r2.status_code == 302
+
+
+def test_gated_require_token_endpoint_accepts_cookie_session(gated_app):
+    """Regression: ``_require_token`` endpoints must work under the OAuth gate.
+
+    In gated mode the legacy ``_SESSION_TOKEN`` is NOT injected into the SPA
+    (it authenticates with the session cookie). Endpoints that call
+    ``_require_token`` directly — plugin install/enable/disable,
+    ``/api/dashboard/plugins/hub``, and others — used to re-check the absent
+    token and 401 every cookie-authenticated request, making them permanently
+    unreachable behind the gate (the dashboard surfaced a
+    ``401: {"detail":"Unauthorized"}`` popup on plugin install). The fix makes
+    ``_require_token`` defer to the gate, which has already verified the cookie
+    and attached ``request.state.session`` before the handler runs.
+
+    We POST a deliberately invalid plugin identifier: a passing auth layer
+    lets the request reach the handler, which rejects the identifier with a
+    400. The assertion is simply "not 401" — proving auth succeeded without
+    coupling to the validation message.
+    """
+    _complete_stub_login(gated_app)
+    r = gated_app.post(
+        "/api/dashboard/agent-plugins/install",
+        json={"identifier": "definitely not a valid identifier",
+              "force": False, "enable": False},
+    )
+    assert r.status_code != 401, (
+        "A _require_token endpoint 401'd a cookie-authenticated request under "
+        f"the OAuth gate (the install-popup bug). Body: {r.text}"
+    )
+    # And specifically: it reached the handler's own validation.
+    assert r.status_code == 400, (
+        f"Expected the install handler's 400 (bad identifier), got "
+        f"{r.status_code}: {r.text}"
+    )
+
+
+def test_gated_require_token_endpoint_still_rejects_no_cookie(gated_app):
+    """The gate must still 401 a ``_require_token`` endpoint with no session.
+
+    The fix defers to the gate — it does not make these endpoints public. A
+    request with no cookie is rejected by ``gated_auth_middleware`` before the
+    handler runs, so the install endpoint stays protected.
+    """
+    r = gated_app.post(
+        "/api/dashboard/agent-plugins/install",
+        json={"identifier": "owner/repo", "force": False, "enable": False},
+    )
+    assert r.status_code == 401, (
+        f"Expected 401 for an unauthenticated install POST under the gate, "
+        f"got {r.status_code}: {r.text}"
+    )
+
+
+# A representative spread of the OTHER ``_require_token`` endpoints (there are
+# 14 in total). The install popup was just the reported symptom; the same bug
+# made API-key reveal, provider validation, the OAuth-provider connect flow,
+# and the rest of plugin management unreachable behind the gate. Each entry is
+# (method, path, json_body); we assert only that a logged-in request is NOT
+# 401'd — i.e. it cleared the auth layer and reached the handler. The
+# handler's own status (400/404/429/etc.) is route-specific and not asserted.
+_GATED_REQUIRE_TOKEN_ROUTES = [
+    ("get", "/api/dashboard/plugins/hub", None),
+    ("post", "/api/env/reveal", {"key": "NONEXISTENT_ENV_VAR_FOR_TEST"}),
+    ("post", "/api/providers/validate", {"key": "OPENAI_API_KEY", "value": ""}),
+    ("delete", "/api/providers/oauth/__not_a_real_provider__", None),
+    ("post", "/api/dashboard/agent-plugins/__nope__/enable", None),
+]
+
+
+@pytest.mark.parametrize("method,path,body", _GATED_REQUIRE_TOKEN_ROUTES)
+def test_gated_require_token_routes_accept_cookie_session(
+    gated_app, method, path, body
+):
+    """Every ``_require_token`` route must clear auth for a logged-in caller.
+
+    Same root cause and fix as
+    ``test_gated_require_token_endpoint_accepts_cookie_session`` — this just
+    proves the fix covers the whole class, not only ``agent-plugins/install``.
+    """
+    _complete_stub_login(gated_app)
+    kwargs = {"json": body} if body is not None else {}
+    r = gated_app.request(method.upper(), path, **kwargs)
+    assert r.status_code != 401, (
+        f"{method.upper()} {path} 401'd a cookie-authenticated request under "
+        f"the OAuth gate — _require_token still rejecting a valid session. "
+        f"Body: {r.text}"
+    )
+
+
 def test_login_unknown_provider_returns_404(gated_app):
     r = gated_app.get("/auth/login?provider=nonexistent", follow_redirects=False)
     assert r.status_code == 404