With vertical tabs enabled, when you remove the last item from the Tab Toolbar it collapses, leaving behind a titlebar sized gap. You are no longer able to add anything back without resetting the toolbars.
As a workaround you could enable the Menu Bar, which is able to make use of the space left behind when the Tab Bar collapses.
Both the Menu Bar and tabless Tab Bar lack any items that fill the center, so you are unable to right-adjust any elements without filling a bunch of Flexible Spaces.
Ideally we should have the option to hide the Tab Bar the same way we can do the Menu Bar, and just let the Navigation Bar move into the titlebar.
Default:
Tab Bar collapsed:
Using the Menu Bar:
Menu Bar + Flexible Space:
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