Sorry for the delay!
So, well, the reason this happens is because this whole thing is super brittle and was basically clinging for its life onto the expectations that nothing would ever change, specifically it is completely reliant on the fact that we immediately discard the prompt when leaving the foreground, which is what bug 1448408 got rid of.
Now, we send an observer notification across the parent process to all open windows, and those will happily show the prompt in their respective selected tab, because we don't have any information about which is the right tab to show the prompt for.
As a super dirty hack we could only show this in the currently visible window, but then what if a background tab tries to show a permission prompt?
This prompt is in a really bad state right now and I would wager that if we can't put resourcing on rewriting the prompting IPC we might need to backout bug 1448408 :/