diff --git a/homeassistant/components/backup/manager.py b/homeassistant/components/backup/manager.py
index bd970d7708a..317de85b823 100644
--- a/homeassistant/components/backup/manager.py
+++ b/homeassistant/components/backup/manager.py
@@ -1620,7 +1620,13 @@ class CoreBackupReaderWriter(BackupReaderWriter):
         """Generate backup contents and return the size."""
         if not tar_file_path:
             tar_file_path = self.temp_backup_dir / f"{backup_data['slug']}.tar"
-        make_backup_dir(tar_file_path.parent)
+        try:
+            make_backup_dir(tar_file_path.parent)
+        except OSError as err:
+            raise BackupReaderWriterError(
+                f"Failed to create dir {tar_file_path.parent}: "
+                f"{err} ({err.__class__.__name__})"
+            ) from err
 
         excludes = EXCLUDE_FROM_BACKUP
         if not database_included:
@@ -1658,7 +1664,14 @@ class CoreBackupReaderWriter(BackupReaderWriter):
                     file_filter=is_excluded_by_filter,
                     arcname="data",
                 )
-        return (tar_file_path, tar_file_path.stat().st_size)
+        try:
+            stat_result = tar_file_path.stat()
+        except OSError as err:
+            raise BackupReaderWriterError(
+                f"Error getting size of {tar_file_path}: "
+                f"{err} ({err.__class__.__name__})"
+            ) from err
+        return (tar_file_path, stat_result.st_size)
 
     async def async_receive_backup(
         self,
diff --git a/tests/components/backup/test_manager.py b/tests/components/backup/test_manager.py
index 3c72929cfe0..6e626e63748 100644
--- a/tests/components/backup/test_manager.py
+++ b/tests/components/backup/test_manager.py
@@ -1311,7 +1311,7 @@ async def test_initiate_backup_with_task_error(
         (1, None, 1, None, 1, None, 1, OSError("Boom!")),
     ],
 )
-async def test_initiate_backup_file_error(
+async def test_initiate_backup_file_error_upload_to_agents(
     hass: HomeAssistant,
     hass_ws_client: WebSocketGenerator,
     generate_backup_id: MagicMock,
@@ -1325,7 +1325,7 @@ async def test_initiate_backup_file_error(
     unlink_call_count: int,
     unlink_exception: Exception | None,
 ) -> None:
-    """Test file error during generate backup."""
+    """Test file error during generate backup, while uploading to agents."""
     agent_ids = ["test.remote"]
 
     await setup_backup_integration(hass, remote_agents=["test.remote"])
@@ -1418,6 +1418,122 @@ async def test_initiate_backup_file_error(
     assert unlink_mock.call_count == unlink_call_count
 
 
+@pytest.mark.usefixtures("mock_backup_generation")
+@pytest.mark.parametrize(
+    (
+        "mkdir_call_count",
+        "mkdir_exception",
+        "atomic_contents_add_call_count",
+        "atomic_contents_add_exception",
+        "stat_call_count",
+        "stat_exception",
+        "error_message",
+    ),
+    [
+        (1, OSError("Boom!"), 0, None, 0, None, "Failed to create dir"),
+        (1, None, 1, OSError("Boom!"), 0, None, "Boom!"),
+        (1, None, 1, None, 1, OSError("Boom!"), "Error getting size"),
+    ],
+)
+async def test_initiate_backup_file_error_create_backup(
+    hass: HomeAssistant,
+    hass_ws_client: WebSocketGenerator,
+    generate_backup_id: MagicMock,
+    path_glob: MagicMock,
+    caplog: pytest.LogCaptureFixture,
+    mkdir_call_count: int,
+    mkdir_exception: Exception | None,
+    atomic_contents_add_call_count: int,
+    atomic_contents_add_exception: Exception | None,
+    stat_call_count: int,
+    stat_exception: Exception | None,
+    error_message: str,
+) -> None:
+    """Test file error during generate backup, while creating backup."""
+    agent_ids = ["test.remote"]
+
+    await setup_backup_integration(hass, remote_agents=["test.remote"])
+
+    ws_client = await hass_ws_client(hass)
+
+    path_glob.return_value = []
+
+    await ws_client.send_json_auto_id({"type": "backup/info"})
+    result = await ws_client.receive_json()
+
+    assert result["success"] is True
+    assert result["result"] == {
+        "backups": [],
+        "agent_errors": {},
+        "last_attempted_automatic_backup": None,
+        "last_completed_automatic_backup": None,
+        "last_non_idle_event": None,
+        "next_automatic_backup": None,
+        "next_automatic_backup_additional": False,
+        "state": "idle",
+    }
+
+    await ws_client.send_json_auto_id({"type": "backup/subscribe_events"})
+
+    result = await ws_client.receive_json()
+    assert result["event"] == {"manager_state": BackupManagerState.IDLE}
+
+    result = await ws_client.receive_json()
+    assert result["success"] is True
+
+    with (
+        patch(
+            "homeassistant.components.backup.manager.atomic_contents_add",
+            side_effect=atomic_contents_add_exception,
+        ) as atomic_contents_add_mock,
+        patch("pathlib.Path.mkdir", side_effect=mkdir_exception) as mkdir_mock,
+        patch("pathlib.Path.stat", side_effect=stat_exception) as stat_mock,
+    ):
+        await ws_client.send_json_auto_id(
+            {"type": "backup/generate", "agent_ids": agent_ids}
+        )
+
+        result = await ws_client.receive_json()
+        assert result["event"] == {
+            "manager_state": BackupManagerState.CREATE_BACKUP,
+            "reason": None,
+            "stage": None,
+            "state": CreateBackupState.IN_PROGRESS,
+        }
+        result = await ws_client.receive_json()
+        assert result["success"] is True
+
+        backup_id = result["result"]["backup_job_id"]
+        assert backup_id == generate_backup_id.return_value
+
+        await hass.async_block_till_done()
+
+    result = await ws_client.receive_json()
+    assert result["event"] == {
+        "manager_state": BackupManagerState.CREATE_BACKUP,
+        "reason": None,
+        "stage": CreateBackupStage.HOME_ASSISTANT,
+        "state": CreateBackupState.IN_PROGRESS,
+    }
+
+    result = await ws_client.receive_json()
+    assert result["event"] == {
+        "manager_state": BackupManagerState.CREATE_BACKUP,
+        "reason": "upload_failed",
+        "stage": None,
+        "state": CreateBackupState.FAILED,
+    }
+
+    result = await ws_client.receive_json()
+    assert result["event"] == {"manager_state": BackupManagerState.IDLE}
+
+    assert atomic_contents_add_mock.call_count == atomic_contents_add_call_count
+    assert mkdir_mock.call_count == mkdir_call_count
+    assert stat_mock.call_count == stat_call_count
+
+    assert error_message in caplog.text
+
+
 def _mock_local_backup_agent(name: str) -> Mock:
     local_agent = mock_backup_agent(name)
     # This makes the local_agent pass isinstance checks for LocalBackupAgent