So this is likely not an issue related to IPv6 and instead the result of misleading error messages - source:

This error is a red herring. if your system does not have IPv6 connectivity, the system first uses IPv4 to communicate, then IPv6 if IPv4 failed. It then for some reason only prints the last line of the output, hiding the IPv4 error

Add the property debug and set it to true inside daemon.json

Unfortunately, even with debug enabled, you may find that the docker logs are not helpful (as was the case for me).

I also encountered this issue and in my specific case my home router was returning malformed DNS responses to name (I think related to eDNS responses). For my particular case, changing my server's DNS servers to point to external DNS resolvers resolved the issues and is probably a good starting point for debugging.

I suspect that the root cause is specifically DNS issues where the A (IPv4) records fail to resolve so the underlying HTTP library attempts to fallback on AAAA (IPV6).

I'm assuming that OP has found some kind of work around or resolution, but leaving this here to help others who have similar issues with docker attempting to use IPv6.