diff --git a/Lib/mailbox.py b/Lib/mailbox.py
index 99426220154360b..510330fcdff54b6 100644
--- a/Lib/mailbox.py
+++ b/Lib/mailbox.py
@@ -18,6 +18,8 @@
 import email.generator
 import io
 import contextlib
+import shutil
+import tempfile
 from types import GenericAlias
 try:
     import fcntl
@@ -1073,8 +1075,11 @@ def __setitem__(self, key, message):
             if self._locked:
                 _lock_file(f)
             try:
-                os.close(os.open(path, os.O_WRONLY | os.O_TRUNC))
-                self._dump_message(message, f)
+                with tempfile.TemporaryFile(mode='w+b') as new_file:
+                    self._dump_message(message, new_file)
+                    new_file.seek(0)
+                    os.close(os.open(path, os.O_WRONLY | os.O_TRUNC))
+                    shutil.copyfileobj(new_file, f)
                 if isinstance(message, MHMessage):
                     self._dump_sequences(message, key)
             finally:
diff --git a/Lib/test/test_mailbox.py b/Lib/test/test_mailbox.py
index 019c699bff55c42..c864a08d695540a 100644
--- a/Lib/test/test_mailbox.py
+++ b/Lib/test/test_mailbox.py
@@ -1,4 +1,5 @@
 import os
+import stat
 import sys
 import time
 import socket
@@ -1338,6 +1339,68 @@ class TestMH(TestMailbox, unittest.TestCase):
     def assertMailboxEmpty(self):
         self.assertEqual(os.listdir(self._path), ['.mh_sequences'])
 
+    def test_set_item_nonascii_string_raises_without_modifying_message(self):
+        key = self._box.add(self._template % 'original')
+        original = self._box.get_bytes(key)
+        with self.assertRaisesRegex(ValueError, "ASCII-only"):
+            self._box[key] = self._nonascii_msg
+        self.assertEqual(self._box.get_bytes(key), original)
+        self._box.close()
+        self._box = self._factory(self._path)
+        self.assertEqual(self._box.get_bytes(key), original)
+
+    def test_set_item_read_error_does_not_modify_message(self):
+        class CustomError(Exception):
+            pass
+
+        class FaultyMessage:
+            def __init__(self):
+                self.first_read = True
+
+            def read(self):
+                raise AssertionError
+
+            def readline(self):
+                if self.first_read:
+                    self.first_read = False
+                    return b'Subject: replacement\n'
+                raise CustomError
+
+        key = self._box.add(self._template % 'original')
+        original = self._box.get_bytes(key)
+        original_files = set(os.listdir(self._path))
+        with self.assertRaises(CustomError):
+            self._box[key] = FaultyMessage()
+        self.assertEqual(self._box.get_bytes(key), original)
+        self.assertEqual(set(os.listdir(self._path)), original_files)
+        self._box.close()
+        self._box = self._factory(self._path)
+        self.assertEqual(self._box.get_bytes(key), original)
+
+    @unittest.skipUnless(os.name == 'posix', 'requires POSIX permissions')
+    def test_set_item_preserves_mode(self):
+        key = self._box.add(self._template % 'original')
+        path = os.path.join(self._path, str(key))
+        mode = 0o640
+        os.chmod(path, mode)
+        if stat.S_IMODE(os.stat(path).st_mode) != mode:
+            self.skipTest('filesystem does not support POSIX permissions')
+
+        self._box[key] = self._template % 'replacement'
+
+        self.assertEqual(stat.S_IMODE(os.stat(path).st_mode), mode)
+
+    def test_set_item_with_open_file(self):
+        key = self._box.add(self._template % 'original')
+        replacement = self._template % 'replacement'
+        self._box.lock()
+        try:
+            with self._box.get_file(key):
+                self._box[key] = replacement
+            self.assertEqual(self._box.get_bytes(key), replacement.encode('ascii'))
+        finally:
+            self._box.unlock()
+
     def test_list_folders(self):
         # List folders
         self._box.add_folder('one')
diff --git a/Misc/NEWS.d/next/Library/2026-08-24-19-37-56.gh-issue-156312.tF9p9m.rst b/Misc/NEWS.d/next/Library/2026-08-24-19-37-56.gh-issue-156312.tF9p9m.rst
new file mode 100644
index 000000000000000..9fcfc2c6a0a8d6f
--- /dev/null
+++ b/Misc/NEWS.d/next/Library/2026-08-24-19-37-56.gh-issue-156312.tF9p9m.rst
@@ -0,0 +1,3 @@
+Prevent :class:`mailbox.MH` message replacement from truncating or partially
+overwriting the original message when serializing the replacement raises an
+exception.