Interesting - I was testing GNOME Boxes and Virtual Machine Manager on Fedora 29 Workstation the other day with Linux VMs. Both were installed from Fedora repos, not flatpaks.
I was able to get an openSUSE Tumbleweed VM to work with both VMM and Boxes, but Ubuntu 18.04.2 LTS was unusable with either hosting, with symptoms very much like what you describe for Windows guests.
Here’s the kicker - on Arch Linux both VMM and Boxes host an Ubuntu VM just fine. I think it’s a “virtual GPU” issue. I’ve also heard of similar problems with Windows 10 Pro Hyper-V hosting Ubuntu VMs - you have to serve RDP from the Ubuntu guest to get a usable display in Hyper-V.
For reference, on the Arch system virt-manager is 2.1.0-2 and gnome-boxes is 3.30.3-1. All tests on both F29 and Arch were run with Wayland disabled on the host.