https://bugs.winehq.org/show_bug.cgi?id=53910
--- Comment #19 from Rafał Mużyło galtgendo@o2.pl --- OK, so I still don't know how to reliably trigger the problem, but it seems I have the recovery nailed down: minimize the affected windows, toggle the secondary (though likely primary would work too, but getting the other windows back in their proper place would take too long) off/on then restore the minimized windows.
So, it's some kind of caching problem with the desktop size (likely due to above mentioned flakiness of the secondary monitor's EDID)...