I am able to reproduce this problem now. It appears to be due to having tabs instead of separate windows and is clearly a macOS bug. I will try to figure out a way to work around this issue. In the intervening time, if you are running into this issue, the simplest way to avoid is to turn off the Tabbed Window preference in Nitro Settings.
If you look at the line between the sidebar and below the toolbar, this is what it should look like:
However, when the bug triggers, the same area is missing the line because it has moved down.
This is not a line that my app draws – this is the responsibility of macOS. Anyway, I will look for a way to avoid it.