diff --git a/litellm/proxy/config_resolvers/settings_store.py b/litellm/proxy/config_resolvers/settings_store.py
index 98ebfdabd0f..345f00c35a5 100644
--- a/litellm/proxy/config_resolvers/settings_store.py
+++ b/litellm/proxy/config_resolvers/settings_store.py
@@ -117,12 +117,13 @@ class SettingsStore(MutableMapping[str, JsonValue]):
         self._deleted_runtime_keys = frozenset()
 
     def _clear_runtime_keys(self, keys: frozenset[str]) -> None:
-        if not keys:
+        stale: Final = frozenset(key for key in keys if not self.owned_by_config(key))
+        if not stale:
             return
         self._runtime_values = MappingProxyType(
-            {key: value for key, value in self._runtime_values.items() if key not in keys}
+            {key: value for key, value in self._runtime_values.items() if key not in stale}
         )
-        self._deleted_runtime_keys = self._deleted_runtime_keys - keys
+        self._deleted_runtime_keys = self._deleted_runtime_keys - stale
 
     def _keys(self) -> tuple[str, ...]:
         return tuple(
diff --git a/tests/test_litellm/proxy/config_resolvers/test_settings_store.py b/tests/test_litellm/proxy/config_resolvers/test_settings_store.py
index 18cbc3b0d6f..1182bcdce3c 100644
--- a/tests/test_litellm/proxy/config_resolvers/test_settings_store.py
+++ b/tests/test_litellm/proxy/config_resolvers/test_settings_store.py
@@ -86,7 +86,6 @@ def test_settings_store_keeps_unaffected_runtime_values_on_a_db_row_refresh() ->
 def test_settings_store_keeps_a_config_owned_key_when_a_db_row_disagrees() -> None:
     store: Final = SettingsStore("general_settings")
     store.load_yaml({"changed": "config"})
-    store.apply_runtime_values({"changed": "resolved-config"})
 
     store.apply_db_row("general_settings", {"changed": "database"})
 
@@ -94,6 +93,17 @@ def test_settings_store_keeps_a_config_owned_key_when_a_db_row_disagrees() -> No
     assert store.source("changed") == "config"
 
 
+def test_settings_store_keeps_the_resolved_value_of_a_config_owned_key_across_a_db_row() -> None:
+    store: Final = SettingsStore("general_settings")
+    store.load_yaml({"changed": "os.environ/SETTING"})
+    store.apply_runtime_values({"changed": "resolved-config"})
+
+    store.apply_db_row("general_settings", {"changed": "database"})
+
+    assert store["changed"] == "resolved-config"
+    assert store.source("changed") == "config"
+
+
 def test_settings_store_removes_only_runtime_values_affected_by_a_cleared_db_row() -> None:
     store: Final = SettingsStore("general_settings")
     store.load_yaml({"template": "os.environ/SETTING"})
diff --git a/tests/test_litellm/proxy/test_proxy_server.py b/tests/test_litellm/proxy/test_proxy_server.py
index 0d59b022e38..d5719a8382c 100644
--- a/tests/test_litellm/proxy/test_proxy_server.py
+++ b/tests/test_litellm/proxy/test_proxy_server.py
@@ -3381,6 +3381,24 @@ async def test_db_reload_finishes_when_the_config_owns_a_setting_the_db_also_set
     assert proxy_config.settings["user_api_key_cache_max_size"] == config_cache_size
 
 
+@pytest.mark.asyncio
+async def test_db_reload_keeps_the_resolved_value_of_a_config_owned_env_reference(monkeypatch):
+    from litellm.proxy import proxy_server as proxy_server_module
+    from litellm.proxy.proxy_server import ProxyConfig
+
+    monkeypatch.setattr(proxy_server_module, "user_api_key_cache", MagicMock(), raising=False)
+    monkeypatch.setattr(proxy_server_module, "store_model_in_db", True, raising=False)
+    proxy_config: Final = ProxyConfig()
+    proxy_config.settings.load_yaml({"store_model_in_db": "os.environ/PROOF_STORE_FLAG"})
+    proxy_config.settings.apply_runtime_values({"store_model_in_db": True})
+    monkeypatch.setattr(proxy_server_module, "general_settings", proxy_config.settings, raising=False)
+
+    await proxy_config._update_general_settings({"store_model_in_db": True})
+
+    assert proxy_config.settings["store_model_in_db"] is True
+    assert proxy_server_module.store_model_in_db is True
+
+
 def test_max_ui_session_budget_default_is_one_dollar():
     """LIT-4662: the dashboard session budget default is a product decision; the
     old 0.25 default locked admins out of auto router Test Connection and the