diff --git a/homeassistant/components/hassio/const.py b/homeassistant/components/hassio/const.py
index b495745e87d..b31c0f1cf15 100644
--- a/homeassistant/components/hassio/const.py
+++ b/homeassistant/components/hassio/const.py
@@ -19,6 +19,7 @@ ATTR_HOMEASSISTANT = "homeassistant"
 ATTR_HOMEASSISTANT_EXCLUDE_DATABASE = "homeassistant_exclude_database"
 ATTR_INPUT = "input"
 ATTR_ISSUES = "issues"
+ATTR_MESSAGE = "message"
 ATTR_METHOD = "method"
 ATTR_PANELS = "panels"
 ATTR_PASSWORD = "password"
diff --git a/homeassistant/components/hassio/handler.py b/homeassistant/components/hassio/handler.py
index 9b8e6367647..65c0824dbd2 100644
--- a/homeassistant/components/hassio/handler.py
+++ b/homeassistant/components/hassio/handler.py
@@ -21,7 +21,7 @@ from homeassistant.const import SERVER_PORT
 from homeassistant.core import HomeAssistant
 from homeassistant.loader import bind_hass
 
-from .const import ATTR_DISCOVERY, DOMAIN, X_HASS_SOURCE
+from .const import ATTR_DISCOVERY, ATTR_MESSAGE, ATTR_RESULT, DOMAIN, X_HASS_SOURCE
 
 _P = ParamSpec("_P")
 
@@ -576,7 +576,7 @@ class HassIO:
             raise HassioAPIError()
 
         try:
-            request = await self.websession.request(
+            response = await self.websession.request(
                 method,
                 joined_url,
                 json=payload,
@@ -589,14 +589,23 @@ class HassIO:
                 timeout=aiohttp.ClientTimeout(total=timeout),
             )
 
-            if request.status != HTTPStatus.OK:
-                _LOGGER.error("%s return code %d", command, request.status)
+            if response.status != HTTPStatus.OK:
+                error = await response.json(encoding="utf-8")
+                if error.get(ATTR_RESULT) == "error":
+                    raise HassioAPIError(error.get(ATTR_MESSAGE))
+
+                _LOGGER.error(
+                    "Request to %s method %s returned with code %d",
+                    command,
+                    method,
+                    response.status,
+                )
                 raise HassioAPIError()
 
             if return_text:
-                return await request.text(encoding="utf-8")
+                return await response.text(encoding="utf-8")
 
-            return await request.json(encoding="utf-8")
+            return await response.json(encoding="utf-8")
 
         except TimeoutError:
             _LOGGER.error("Timeout on %s request", command)
diff --git a/homeassistant/components/hassio/websocket_api.py b/homeassistant/components/hassio/websocket_api.py
index cf59f8de7f7..13c258dd68c 100644
--- a/homeassistant/components/hassio/websocket_api.py
+++ b/homeassistant/components/hassio/websocket_api.py
@@ -21,7 +21,6 @@ from .const import (
     ATTR_DATA,
     ATTR_ENDPOINT,
     ATTR_METHOD,
-    ATTR_RESULT,
     ATTR_SESSION_DATA_USER_ID,
     ATTR_TIMEOUT,
     ATTR_WS_EVENT,
@@ -131,9 +130,6 @@ async def websocket_supervisor_api(
             payload=payload,
             source="core.websocket_api",
         )
-
-        if result.get(ATTR_RESULT) == "error":
-            raise HassioAPIError(result.get("message"))
     except HassioAPIError as err:
         _LOGGER.error("Failed to to call %s - %s", msg[ATTR_ENDPOINT], err)
         connection.send_error(
diff --git a/tests/components/hassio/test_websocket_api.py b/tests/components/hassio/test_websocket_api.py
index b2f9e06cb43..ee17ad62e74 100644
--- a/tests/components/hassio/test_websocket_api.py
+++ b/tests/components/hassio/test_websocket_api.py
@@ -171,6 +171,7 @@ async def test_websocket_supervisor_api_error(
     aioclient_mock.get(
         "http://127.0.0.1/ping",
         json={"result": "error", "message": "example error"},
+        status=400,
     )
 
     await websocket_client.send_json(
@@ -183,9 +184,39 @@ async def test_websocket_supervisor_api_error(
     )
 
     msg = await websocket_client.receive_json()
+    assert msg["error"]["code"] == "unknown_error"
     assert msg["error"]["message"] == "example error"
 
 
+async def test_websocket_supervisor_api_error_without_msg(
+    hassio_env,
+    hass: HomeAssistant,
+    hass_ws_client: WebSocketGenerator,
+    aioclient_mock: AiohttpClientMocker,
+) -> None:
+    """Test Supervisor websocket api error."""
+    assert await async_setup_component(hass, "hassio", {})
+    websocket_client = await hass_ws_client(hass)
+    aioclient_mock.get(
+        "http://127.0.0.1/ping",
+        json={},
+        status=400,
+    )
+
+    await websocket_client.send_json(
+        {
+            WS_ID: 1,
+            WS_TYPE: WS_TYPE_API,
+            ATTR_ENDPOINT: "/ping",
+            ATTR_METHOD: "get",
+        }
+    )
+
+    msg = await websocket_client.receive_json()
+    assert msg["error"]["code"] == "unknown_error"
+    assert msg["error"]["message"] == ""
+
+
 async def test_websocket_non_admin_user(
     hassio_env,
     hass: HomeAssistant,