diff --git a/gateway/config.py b/gateway/config.py
index cc80cda40155..b43485fefeb9 100644
--- a/gateway/config.py
+++ b/gateway/config.py
@@ -2011,7 +2011,19 @@ def _apply_env_overrides(config: GatewayConfig) -> None:
     if api_server_enabled or api_server_key:
         if Platform.API_SERVER not in config.platforms:
             config.platforms[Platform.API_SERVER] = PlatformConfig()
-        config.platforms[Platform.API_SERVER].enabled = True
+        # Respect an explicit ``enabled: false`` in config.yaml (flagged by
+        # ``_enabled_explicit``). In multiplex mode a secondary profile's
+        # config.yaml pins ``platforms.api_server.enabled: false`` so it shares
+        # the default profile's listener instead of binding its own port. That
+        # profile still inherits the process-level env (including
+        # ``API_SERVER_KEY``); without this guard the env-var presence would
+        # force-enable the listener and trip the MultiplexConfigError check.
+        # Pop (don't read) the marker — the api_server branch is terminal (no
+        # later registry pass re-enables it), so this both consumes the flag and
+        # avoids reading it twice, matching the pop convention used elsewhere.
+        api_server_explicit = config.platforms[Platform.API_SERVER].extra.pop("_enabled_explicit", False)
+        if not api_server_explicit or config.platforms[Platform.API_SERVER].enabled:
+            config.platforms[Platform.API_SERVER].enabled = True
         if api_server_key:
             config.platforms[Platform.API_SERVER].extra["key"] = api_server_key
         if api_server_cors_origins:
diff --git a/tests/gateway/test_config.py b/tests/gateway/test_config.py
index 910961dd7bf1..0b272ab74eb8 100644
--- a/tests/gateway/test_config.py
+++ b/tests/gateway/test_config.py
@@ -2117,3 +2117,36 @@ class TestMultiplexProfilesConfig:
             "Explicit top-level false was overridden by nested true — "
             "loader must respect top-level precedence when key is present"
         )
+
+
+class TestApiServerEnvOverride:
+    def test_env_key_does_not_reenable_explicitly_disabled_api_server(self):
+        """An explicit ``platforms.api_server.enabled: false`` must survive
+        _apply_env_overrides() even when API_SERVER_KEY is present in the env.
+
+        Regression: _apply_env_overrides() force-set api_server.enabled = True
+        whenever API_SERVER_KEY (or API_SERVER_ENABLED) was set. In multiplex
+        mode a secondary profile pins ``api_server.enabled: false`` so it shares
+        the default profile's listener instead of binding its own port, but it
+        still inherits the process-level API_SERVER_KEY. The unconditional
+        re-enable flipped it back on and tripped the MultiplexConfigError check.
+
+        The fix honors the explicit disable, flagged by ``_enabled_explicit`` in
+        the platform's extra (set when the config.yaml pins enabled).
+        """
+        config = GatewayConfig(
+            platforms={
+                Platform.API_SERVER: PlatformConfig(
+                    enabled=False,
+                    extra={"_enabled_explicit": True},
+                ),
+            },
+        )
+
+        with patch.dict(os.environ, {"API_SERVER_KEY": "secret-key"}, clear=True):
+            _apply_env_overrides(config)
+
+        # Explicit disable wins over the env-var presence.
+        assert config.platforms[Platform.API_SERVER].enabled is False
+        # The key is still wired through for the shared listener.
+        assert config.platforms[Platform.API_SERVER].extra.get("key") == "secret-key"