diff --git a/homeassistant/components/hassio/backup.py b/homeassistant/components/hassio/backup.py
index 1b7cf930588..ad3bd78adec 100644
--- a/homeassistant/components/hassio/backup.py
+++ b/homeassistant/components/hassio/backup.py
@@ -28,6 +28,9 @@ from homeassistant.components.backup import (
     NewBackup,
     WrittenBackup,
 )
+
+# pylint: disable-next=hass-component-root-import
+from homeassistant.components.backup.manager import IncorrectPasswordError
 from homeassistant.core import HomeAssistant, callback
 from homeassistant.exceptions import HomeAssistantError
 from homeassistant.helpers.dispatcher import async_dispatcher_connect
@@ -385,17 +388,24 @@ class SupervisorBackupReaderWriter(BackupReaderWriter):
             agent = cast(SupervisorBackupAgent, manager.backup_agents[agent_id])
             restore_location = agent.location
 
-        job = await self._client.backups.partial_restore(
-            backup_id,
-            supervisor_backups.PartialRestoreOptions(
-                addons=restore_addons_set,
-                folders=restore_folders_set,
-                homeassistant=restore_homeassistant,
-                password=password,
-                background=True,
-                location=restore_location,
-            ),
-        )
+        try:
+            job = await self._client.backups.partial_restore(
+                backup_id,
+                supervisor_backups.PartialRestoreOptions(
+                    addons=restore_addons_set,
+                    folders=restore_folders_set,
+                    homeassistant=restore_homeassistant,
+                    password=password,
+                    background=True,
+                    location=restore_location,
+                ),
+            )
+        except SupervisorBadRequestError as err:
+            # Supervisor currently does not transmit machine parsable error types
+            message = err.args[0]
+            if message.startswith("Invalid password for backup"):
+                raise IncorrectPasswordError(message) from err
+            raise HomeAssistantError(message) from err
 
         restore_complete = asyncio.Event()
 
diff --git a/tests/components/hassio/test_backup.py b/tests/components/hassio/test_backup.py
index 3c9440c41ff..450c9ddded9 100644
--- a/tests/components/hassio/test_backup.py
+++ b/tests/components/hassio/test_backup.py
@@ -997,6 +997,77 @@ async def test_reader_writer_restore(
     assert response["result"] is None
 
 
+@pytest.mark.parametrize(
+    ("supervisor_error_string", "expected_error_code"),
+    [
+        (
+            "Invalid password for backup",
+            "password_incorrect",
+        ),
+        (
+            "Backup was made on supervisor version 2025.12.0, can't restore on 2024.12.0. Must update supervisor first.",
+            "home_assistant_error",
+        ),
+    ],
+)
+@pytest.mark.usefixtures("hassio_client", "setup_integration")
+async def test_reader_writer_restore_error(
+    hass: HomeAssistant,
+    hass_ws_client: WebSocketGenerator,
+    supervisor_client: AsyncMock,
+    supervisor_error_string: str,
+    expected_error_code: str,
+) -> None:
+    """Test restoring a backup."""
+    client = await hass_ws_client(hass)
+    supervisor_client.backups.partial_restore.side_effect = SupervisorBadRequestError(
+        supervisor_error_string
+    )
+    supervisor_client.backups.list.return_value = [TEST_BACKUP]
+    supervisor_client.backups.backup_info.return_value = TEST_BACKUP_DETAILS
+
+    await client.send_json_auto_id({"type": "backup/subscribe_events"})
+    response = await client.receive_json()
+    assert response["event"] == {"manager_state": "idle"}
+    response = await client.receive_json()
+    assert response["success"]
+
+    await client.send_json_auto_id(
+        {"type": "backup/restore", "agent_id": "hassio.local", "backup_id": "abc123"}
+    )
+    response = await client.receive_json()
+    assert response["event"] == {
+        "manager_state": "restore_backup",
+        "stage": None,
+        "state": "in_progress",
+    }
+
+    supervisor_client.backups.partial_restore.assert_called_once_with(
+        "abc123",
+        supervisor_backups.PartialRestoreOptions(
+            addons=None,
+            background=True,
+            folders=None,
+            homeassistant=True,
+            location=None,
+            password=None,
+        ),
+    )
+
+    response = await client.receive_json()
+    assert response["event"] == {
+        "manager_state": "restore_backup",
+        "stage": None,
+        "state": "failed",
+    }
+
+    response = await client.receive_json()
+    assert response["event"] == {"manager_state": "idle"}
+
+    response = await client.receive_json()
+    assert response["error"]["code"] == expected_error_code
+
+
 @pytest.mark.parametrize(
     ("parameters", "expected_error"),
     [