Yet another example of the digital h̶u̶m̶i̶l̶a̶t̶i̶o̶n̶ experience for editors using Plone:
I doubt that there should be any difference between second and third time because of the Widget.
I would guess that the reason is that you are using the widget within a portlet, and because of that something is messed up 'stylewise. For example: the z-index moves it in front of everything in right column, but not of everything in main column.
Similar things also happens when you have a popup inside another popup
Most likely this would not be a problem if it was used in 'main content'.
I would guess you could fix this by adding z-index to 'the popup or something else'.
Another option could be to render the right column before main column and then move it to the right with css ( flex order of float right or css classes).
I would check if the same thing happens if you place the portlet in left column or footer portets
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Also added to the issue on github:
@zopyx The issue is not exactly the same, but I encountered multiple problems with TinyMCE menu's disappaering last year, the common pattern here is the modal pattern from Mockup.
See these two issues:
I only see the scroll position of the whole page slightly in your third screenshot. Can you confirm that the scroll position of the whole page is related to the shifting of the content list in the related items widget in the modal?