diff --git a/Lib/mailbox.py b/Lib/mailbox.py
index 0efd7434fee..6a69819c968 100644
--- a/Lib/mailbox.py
+++ b/Lib/mailbox.py
@@ -649,6 +649,7 @@ class _singlefileMailbox(Mailbox):
                     new_file.write(buffer)
                 new_toc[key] = (new_start, new_file.tell())
                 self._post_message_hook(new_file)
+            self._file_length = new_file.tell()
         except:
             new_file.close()
             os.remove(new_file.name)
diff --git a/Lib/test/test_mailbox.py b/Lib/test/test_mailbox.py
index 480d586143c..6ebd1a29bd9 100644
--- a/Lib/test/test_mailbox.py
+++ b/Lib/test/test_mailbox.py
@@ -386,6 +386,17 @@ class TestMailbox(TestBase):
         # Write changes to disk
         self._test_flush_or_close(self._box.flush, True)
 
+    def test_popitem_and_flush_twice(self):
+        # See #15036.
+        self._box.add(self._template % 0)
+        self._box.add(self._template % 1)
+        self._box.flush()
+
+        self._box.popitem()
+        self._box.flush()
+        self._box.popitem()
+        self._box.flush()
+
     def test_lock_unlock(self):
         # Lock and unlock the mailbox
         self.assertFalse(os.path.exists(self._get_lock_path()))
diff --git a/Misc/NEWS b/Misc/NEWS
index c4010c3c34c..c4b27fb8f05 100644
--- a/Misc/NEWS
+++ b/Misc/NEWS
@@ -67,6 +67,10 @@ Core and Builtins
 Library
 -------
 
+- Issue #15036: Allow removing or changing multiple items in
+  single-file mailboxes (mbox, MMDF, Babyl) flushing the mailbox
+  between the changes.
+
 - Issue #10133: Make multiprocessing deallocate buffer if socket read
   fails.  Patch by Hallvard B Furuseth.