I believe my problems were caused my trying to run the VM on top of whatever else is going on. Disabling VM's has eliminated all weird bugs. It's possible the culprit was the unsupported video card. I have since tried an unofficial kernel that adds drivers for the video card and it has been playing well with Docker containers thus far. I'm going to go ahead and mark this thread as resolved, with the solution being don't use VM's with new hardware!
