I have GNOME terminal and Emacs client, in the same AppVM (not that this should matter), running side by side. I will switch windows with alt+tab from Emacs to the terminal (though the problem persists with clicking to change focus as well) and the title bar of the terminal will clearly gain focus. However, anything I type will still be sent to Emacs. I often have to minimize Emacs or highlight part of GNOME terminal for it to actually accept my input.

I have run qubes-dom0-update, but the problem persists.

I tried to submit this as a ticket, but qubes-os.org insists there is some CAPTCHA that I cannot see even w/o my browser add-ons enabled.