diff --git a/litellm/proxy/anthropic_endpoints/gateway_endpoints.py b/litellm/proxy/anthropic_endpoints/gateway_endpoints.py
index 991dc67ab82..cc3106fce53 100644
--- a/litellm/proxy/anthropic_endpoints/gateway_endpoints.py
+++ b/litellm/proxy/anthropic_endpoints/gateway_endpoints.py
@@ -80,6 +80,12 @@ class _AccessTokenBody(BaseModel):
     token_type: str = "Bearer"
 
 
+class _ManagedSettingsBody(BaseModel):
+    uuid: str
+    checksum: str
+    settings: dict[str, object]
+
+
 def _general_settings() -> Mapping[str, object]:
     from litellm.proxy.proxy_server import general_settings
 
@@ -333,12 +339,14 @@ async def managed_settings(request: Request) -> Response:
     if settings is None:
         return Response(status_code=404)
 
-    body: Final = json.dumps(settings, sort_keys=True, separators=(",", ":"))
-    etag: Final = '"' + hashlib.sha256(body.encode("utf-8")).hexdigest() + '"'
+    canonical: Final = json.dumps(settings, sort_keys=True, separators=(",", ":"))
+    checksum: Final = "sha256:" + hashlib.sha256(canonical.encode("utf-8")).hexdigest()
+    etag: Final = f'"{checksum}"'
     headers: Final = MappingProxyType({"ETag": etag})
     if request.headers.get("If-None-Match") == etag:
         return Response(status_code=304, headers=headers)
-    return Response(content=body, media_type="application/json", headers=headers)
+    body: Final = _ManagedSettingsBody(uuid=checksum, checksum=checksum, settings=settings)
+    return Response(content=body.model_dump_json(), media_type="application/json", headers=headers)
 
 
 def _accept_otlp() -> Response:
diff --git a/tests/test_litellm/proxy/anthropic_endpoints/test_gateway_endpoints.py b/tests/test_litellm/proxy/anthropic_endpoints/test_gateway_endpoints.py
index c0a39b95c40..158fe253796 100644
--- a/tests/test_litellm/proxy/anthropic_endpoints/test_gateway_endpoints.py
+++ b/tests/test_litellm/proxy/anthropic_endpoints/test_gateway_endpoints.py
@@ -327,18 +327,35 @@ def test_managed_settings_404_when_unset():
     assert resp.status_code == 404
 
 
-def test_managed_settings_returns_json_with_etag_and_304():
+def test_managed_settings_returns_client_envelope_and_304_on_cached_checksum():
     settings = {"permissions": {"defaultMode": "acceptEdits"}, "env": {"FOO": "bar"}}
     with _gateway_env(managed_settings=settings) as (client, _):
         resp = client.get("/claude_code_gateway/managed/settings")
         assert resp.status_code == 200
-        assert resp.json() == settings
-        etag = resp.headers["ETag"]
-        assert etag
+        body = resp.json()
+        assert body["settings"] == settings
+        checksum = body["checksum"]
+        assert checksum.startswith("sha256:")
+        assert body["uuid"] == checksum
+        assert resp.headers["ETag"] == f'"{checksum}"'
 
-        not_modified = client.get("/claude_code_gateway/managed/settings", headers={"If-None-Match": etag})
-    assert not_modified.status_code == 304
-    assert not_modified.headers["ETag"] == etag
+        not_modified = client.get(
+            "/claude_code_gateway/managed/settings", headers={"If-None-Match": f'"{checksum}"'}
+        )
+        assert not_modified.status_code == 304
+        assert not_modified.headers["ETag"] == f'"{checksum}"'
+
+        stale = client.get("/claude_code_gateway/managed/settings", headers={"If-None-Match": '"sha256:stale"'})
+    assert stale.status_code == 200
+    assert stale.json()["checksum"] == checksum
+
+
+def test_managed_settings_checksum_tracks_policy_content():
+    with _gateway_env(managed_settings={"env": {"FOO": "bar"}}) as (client, _):
+        first = client.get("/claude_code_gateway/managed/settings").json()["checksum"]
+    with _gateway_env(managed_settings={"env": {"FOO": "baz"}}) as (client, _):
+        second = client.get("/claude_code_gateway/managed/settings").json()["checksum"]
+    assert first != second
 
 
 def test_managed_settings_404_when_gateway_disabled():