diff --git a/Doc/library/zipfile.rst b/Doc/library/zipfile.rst
index 98d2a5e5cdf00e..d5e9348ec8ba00 100644
--- a/Doc/library/zipfile.rst
+++ b/Doc/library/zipfile.rst
@@ -581,7 +581,9 @@ ZipFile objects
                            strict_descriptor=True[, chunk_size])
 
    Rewrites the archive to remove unreferenced local file entries, shrinking
-   its file size.  The archive must be opened with mode ``'a'``.
+   its file size.  The archive must be opened with mode ``'a'``, and any file
+   object returned by :meth:`ZipFile.open` must be closed first, since
+   repacking moves the member data those objects read from.
 
    If *removed* is provided, it must be a sequence of :class:`ZipInfo` objects
    representing the recently removed members, and only their corresponding
diff --git a/Lib/test/test_zipfile/test_core.py b/Lib/test/test_zipfile/test_core.py
index cd498ba13e6f46..11a01d8daacf4d 100644
--- a/Lib/test/test_zipfile/test_core.py
+++ b/Lib/test/test_zipfile/test_core.py
@@ -2382,6 +2382,18 @@ def test_repack_writing(self, m_repack):
                     zh.repack()
         m_repack.assert_not_called()
 
+    @mock.patch.object(zipfile, '_ZipRepacker')
+    def test_repack_reading(self, m_repack):
+        self._prepare_zip_from_test_files(TESTFN, self.test_files)
+        with zipfile.ZipFile(TESTFN, 'a') as zh:
+            with zh.open(self.test_files[0][0]):
+                with self.assertRaises(ValueError):
+                    zh.repack()
+            m_repack.assert_not_called()
+            # Allowed once the reading handle is closed.
+            zh.repack()
+        m_repack.assert_called_once()
+
     @mock.patch.object(zipfile, '_ZipRepacker')
     def test_repack_mode_r(self, m_repack):
         self._prepare_zip_from_test_files(TESTFN, self.test_files)
diff --git a/Lib/zipfile/__init__.py b/Lib/zipfile/__init__.py
index 418933a2e8d9e8..aea5678ac84c29 100644
--- a/Lib/zipfile/__init__.py
+++ b/Lib/zipfile/__init__.py
@@ -2404,6 +2404,11 @@ def repack(self, removed=None, *, strict_descriptor=True,
             raise ValueError(
                 "Can't write to ZIP archive while an open writing handle exists"
             )
+        if self._fileRefCnt > 1:
+            raise ValueError(
+                "Can't repack the ZIP archive while an open reading handle "
+                "exists. Close the reading handle before repacking."
+            )
 
         with self._lock:
             self._writing = True