Want to add that disconnecting the secondary monitor causes this issue, too. Please see attached image:

Fedora 40
Steam Beta Branch: Steam Beta Update
Steam Version: 1714854927
Same bug manifests when putting computer to sleep and waking up. Restarting steam "solves" the issue.
Steam Beta Branch: Stable Client
Steam Version: 1733265492
Plasma 6.2.4 / KWin (Wayland)
Nothing extracted yet.
Your system information
tar -zcvf ~/Desktop/steam-logs.tar.gz ~/.steam/steam/logs]Please describe your issue in as much detail as possible:
On a fresh started client, all child elements, like menu toolbar boxes, boxes that appear while hovering Store/Library/Community/Profile, and game properties and other child windows, are rendered consistent with the main window in the same non-primary/right monitor. Whenever both monitors are shutdown/disconnected, the main window will be rendered on the screen it is positioned, but the child elements would be created to the right edge of the primary/left screen. Moving the main window to the primary screen doesn't fix the issue, but the child elements are rendered where they should be relative to the main window. Restarting the client does fix the issue.
Steps for reproducing this issue: