Since then I get these errors in some VMs, but not others:
Failed to parse rules for aaaa:bbbb:cccc::ddd:00 (Failed to resolve example.com)
Despite the errors, I can resolv the domain with dig inside the VM, and networking seems to be fine. The error is always for whatever domain I have at the top of the list in the firewall for the VM, like addons.mozilla.org.
Can you confirm if the error stops happening if you disable the feature?
If that is the case then it seems like a straightforward set of steps to reproduce the error, and opening an issue on GitHub could be useful. (After checking that there isn’t one already that describes that behavior.)
If you go that way, it would be useful to mention which version of Qubes OS you’re using. (R4.1 I suppose?)
Edit: It doesn’t seem like the issue has been reported yet (direct link to the filtered list of issues that contain ipv6 and affect R4.1):