StackExchange doesn’t to my knowledge allow pictures in comments, so I’ll post my pictures here in case someone else has more time to reproduce and debug this issue.
Original question (please post any comments there):
https://askubuntu.com/questions/495997/how-to-properly-restart-unity
Original state when I resumed my 2015 Macbook Pro with Ubuntu 16.04.3 LTS and all updates applied from sleep this morning, after plugging and unplugging the HDMI cable a few times:

State after the sudo systemctl restart lightdm.service
command was run:

The second monitor returned to normal after I tried the sudo reboot now
workaround.