This issue can not be reproduced with vanilla Tor Browser on a non-whonix machine so the assumption is that it is somehow related to Whonix even though Whonix does not aim to make changes to Tor Browser, but minor changes to its configuration are required by Whonix (i.e. SOCKS settings, startpage, ..) that could be triggering this issue.
I also noticed the file "~/.tb/first-boot-home-population.done" which suggests that whonix does something on first boot that it does not everytime (which would explain why this happens only on first boot if at all). The issue is particularly annoying on dispVMs based on whonix-ws-14 because there every boot is the "first boot".
Tor Browser Version: 8.0.6 (it also happened with 8.0.5)