> There is no similar function taking a directory handle

In 3.5+ the CRT has O_OBTAIN_DIR (0x2000) for opening a directory, i.e. to call CreateFile with backup semantics. A directory can be read via GetFileInformationByHandleEx [1] using the information classes FileIdBothDirectoryRestartInfo and FileIdBothDirectoryInfo. This info class is just a simplified wrapper around the more powerful system call NtQueryDirectoryFile [2]. 

The implementation details could be hidden behind _Py_opendir, _Py_fdopendir, _Py_readdir, and _Py_closedir -- allowing a common implementation of the high-level listdir() and scandir() functions. I wrote a ctypes prototype of listdir() along these lines.

One feature that's lost in using GetFileInformationByHandleEx to list a directory is the ability to do wildcard filtering. However, Python listdir and scandir never uses wildcard filtering, so it's no real loss. FindFirstFile implements this feature via the FileName parameter of NtQueryDirectoryFile. First it translates DOS wildcards to NT's set of 5 wildcards. There's the native NT '*' and '?', plus the quirky semantics of MS-DOS via '<', '>', and '"', i.e. DOS_STAR, DOS_QM, and DOS_DOT. See FsRtlIsNameInExpression [3] for a description of these wildcard characters. 

[1]: https://msdn.microsoft.com/en-us/library/aa364953
[2]: https://msdn.microsoft.com/en-us/library/ff567047
[3]: https://msdn.microsoft.com/en-us/library/ff546850