diff --git a/homeassistant/components/backup/manager.py b/homeassistant/components/backup/manager.py
index 36791a1915269..5513b912bd653 100644
--- a/homeassistant/components/backup/manager.py
+++ b/homeassistant/components/backup/manager.py
@@ -12,7 +12,6 @@
 from pathlib import Path
 import shutil
 import tarfile
-from tempfile import TemporaryDirectory
 import time
 from typing import TYPE_CHECKING, Any, Protocol
 
@@ -389,25 +388,11 @@ async def async_receive_backup(
         contents: aiohttp.BodyPartReader,
     ) -> None:
         """Receive and store a backup file from upload."""
-        temp_dir_handler = await self.hass.async_add_executor_job(TemporaryDirectory)
-        target_temp_file = Path(
-            temp_dir_handler.name, contents.filename or "backup.tar"
-        )
+        target_temp_file = Path(self.temp_backup_dir, contents.filename or "backup.tar")
+        await self.hass.async_add_executor_job(make_backup_dir, self.temp_backup_dir)
 
         await receive_file(self.hass, contents, target_temp_file)
 
-        def _copy_and_cleanup(
-            local_file_paths: list[Path], backup: AgentBackup
-        ) -> Path:
-            if local_file_paths:
-                tar_file_path = local_file_paths[0]
-            else:
-                tar_file_path = self.temp_backup_dir / f"{backup.backup_id}.tar"
-            for local_path in local_file_paths:
-                shutil.copy(target_temp_file, local_path)
-            temp_dir_handler.cleanup()
-            return tar_file_path
-
         try:
             backup = await self.hass.async_add_executor_job(
                 read_backup, target_temp_file
@@ -421,9 +406,18 @@ def _copy_and_cleanup(
             for agent_id in agent_ids
             if agent_id in self.local_backup_agents
         ]
-        tar_file_path = await self.hass.async_add_executor_job(
-            _copy_and_cleanup, local_file_paths, backup
-        )
+        if local_file_paths:
+
+            def _copy_to_local_agents(local_file_paths: list[Path]) -> Path:
+                for local_path in local_file_paths:
+                    shutil.copy(target_temp_file, local_path)
+                return local_file_paths[0]
+
+            tar_file_path = await self.hass.async_add_executor_job(
+                _copy_to_local_agents, local_file_paths
+            )
+        else:
+            tar_file_path = target_temp_file
         await self._async_upload_backup(
             backup=backup, agent_ids=agent_ids, path=tar_file_path
         )
diff --git a/tests/components/cloud/test_backup.py b/tests/components/cloud/test_backup.py
index faeacbe006c87..41414426f5243 100644
--- a/tests/components/cloud/test_backup.py
+++ b/tests/components/cloud/test_backup.py
@@ -525,6 +525,7 @@ async def test_agents_upload_not_protected(
         size=0.0,
     )
     with (
+        patch("pathlib.Path.open"),
         patch(
             "homeassistant.components.backup.manager.read_backup",
             return_value=test_backup,
diff --git a/tests/components/hassio/test_backup.py b/tests/components/hassio/test_backup.py
index 426329a622b07..07fbd500752cc 100644
--- a/tests/components/hassio/test_backup.py
+++ b/tests/components/hassio/test_backup.py
@@ -184,6 +184,8 @@ async def test_agent_upload(
 
     supervisor_client.backups.reload.assert_not_called()
     with (
+        patch("pathlib.Path.mkdir"),
+        patch("pathlib.Path.open"),
         patch(
             "homeassistant.components.backup.manager.BackupManager.async_get_backup",
         ) as fetch_backup,
diff --git a/tests/components/kitchen_sink/test_backup.py b/tests/components/kitchen_sink/test_backup.py
index d36b287871340..2e53216d43e2c 100644
--- a/tests/components/kitchen_sink/test_backup.py
+++ b/tests/components/kitchen_sink/test_backup.py
@@ -141,6 +141,7 @@ async def test_agents_upload(
     )
 
     with (
+        patch("pathlib.Path.open"),
         patch(
             "homeassistant.components.backup.manager.BackupManager.async_get_backup",
         ) as fetch_backup,