diff --git a/git/config.py b/git/config.py
index 732d3658b..8d011ec8a 100644
--- a/git/config.py
+++ b/git/config.py
@@ -730,7 +730,12 @@ def _all_items(section: str) -> List[Tuple[str, str]]:
             value = match.group(2).strip()
 
             if keyword in ["gitdir", "gitdir/i"]:
-                value = osp.expanduser(value)
+                if sys.platform == "win32" and (value == "~" or value.startswith("~/")):
+                    # Like Git, substitute the home directory with forward slashes, as a
+                    # backslash in the pattern would escape the next character.
+                    value = osp.expanduser("~").replace("\\", "/") + value[1:]
+                else:
+                    value = osp.expanduser(value)
                 git_dir = os.fspath(self._repo.git_dir) if self._repo.git_dir else None
                 if sys.platform == "win32":
                     git_dir = git_dir.replace("\\", "/") if git_dir else None
diff --git a/test/test_config.py b/test/test_config.py
index 49b8535c7..f7907e98e 100644
--- a/test/test_config.py
+++ b/test/test_config.py
@@ -989,6 +989,22 @@ def test_conditional_includes_do_not_treat_backslashes_as_separators(self, rw_di
         with GitConfigParser(config_path, repo=repo, merge_includes=False) as config:
             assert config._included_paths() == []
 
+    @with_rw_directory
+    def test_conditional_includes_expand_home_in_git_dir_pattern(self, rw_dir):
+        git_dir = osp.join(rw_dir, "target", "repo", ".git")
+        repo = mock.Mock(git_dir=git_dir)
+        config_path = osp.join(rw_dir, "config")
+        included_path = osp.join(rw_dir, "included")
+
+        with open(config_path, "w") as stream:
+            stream.write(f'[includeIf "gitdir:~/target/"]\n    path={included_path}\n')
+
+        # On Windows, the home directory has backslashes, but Git matches it as if it
+        # were written with forward slashes.
+        with mock.patch.dict(os.environ, {"HOME": rw_dir, "USERPROFILE": rw_dir}):
+            with GitConfigParser(config_path, repo=repo, merge_includes=False) as config:
+                assert config._included_paths() == [("path", included_path)]
+
     @with_rw_directory
     def test_conditional_includes_from_branch_name(self, rw_dir):
         # Initiate mocked branch.