diff --git a/supervisor/docker/homeassistant.py b/supervisor/docker/homeassistant.py
index 999877af1..c71f6d1d4 100644
--- a/supervisor/docker/homeassistant.py
+++ b/supervisor/docker/homeassistant.py
@@ -184,7 +184,7 @@ class DockerHomeAssistant(DockerInterface):
         }
         if restore_job_id:
             environment[ENV_RESTORE_JOB_ID] = restore_job_id
-        if self.sys_homeassistant.api.use_unix_socket:
+        if self.sys_homeassistant.api.supports_unix_socket:
             environment[ENV_CORE_API_SOCKET] = "/run/supervisor/core.sock"
         if self.sys_homeassistant.duplicate_log_file:
             environment[ENV_DUPLICATE_LOG_FILE] = "1"
diff --git a/supervisor/homeassistant/api.py b/supervisor/homeassistant/api.py
index 49b1ee8aa..e1ccb3231 100644
--- a/supervisor/homeassistant/api.py
+++ b/supervisor/homeassistant/api.py
@@ -15,6 +15,7 @@ from multidict import MultiMapping
 
 from ..const import SOCKET_CORE
 from ..coresys import CoreSys, CoreSysAttributes
+from ..docker.const import ENV_CORE_API_SOCKET
 from ..exceptions import HomeAssistantAPIError, HomeAssistantAuthError
 from ..utils import version_is_new_enough
 from .const import LANDINGPAGE
@@ -51,8 +52,11 @@ class HomeAssistantAPI(CoreSysAttributes):
         self._logged_transport: bool = False
 
     @property
-    def use_unix_socket(self) -> bool:
-        """Return True if Core supports Unix socket communication."""
+    def supports_unix_socket(self) -> bool:
+        """Return True if the installed Core version supports Unix socket communication.
+
+        Used to decide whether to configure the env var when starting Core.
+        """
         return (
             self.sys_homeassistant.version is not None
             and self.sys_homeassistant.version != LANDINGPAGE
@@ -61,6 +65,24 @@ class HomeAssistantAPI(CoreSysAttributes):
             )
         )
 
+    @property
+    def use_unix_socket(self) -> bool:
+        """Return True if the running Core container is configured for Unix socket.
+
+        Checks both version support and that the container was actually started
+        with the SUPERVISOR_CORE_API_SOCKET env var. This prevents failures
+        during Supervisor upgrades where Core is still running with a container
+        started by the old Supervisor.
+        """
+        if not self.supports_unix_socket:
+            return False
+        meta_config = self.sys_homeassistant.core.instance.meta_config
+        if not meta_config or "Env" not in meta_config:
+            return False
+        return any(
+            env.startswith(f"{ENV_CORE_API_SOCKET}=") for env in meta_config["Env"]
+        )
+
     @property
     def session(self) -> aiohttp.ClientSession:
         """Return session for Core communication.