Thanks for the detailed bug report!
I'm currently investigating this; I don't have any particular answers yet, though the problem appears with a regular bar as well as a controller bar, so it seems to be a problem specific to the controller viewport. Strangely, it doesn't always appear either - you'll notice that the bars that come with the preference screen included in the template don't have this problem. I've been able to tentatively narrow it down to something going wrong in the render method. I'll keep plugging away at it when I have time. In the meantime, you might play around with copying over the preference screen controller_bar layout and adjusting it to find a version that works.