I believe you’re correct, that any time you have multiple vagrant VMs running in your development environment, you’ll need to edit the related vagrantfiles to have unique IPs (before vagrant up). There is some discussion here and at roots/trellis#295.
You won’t need to worry about IPs for VMs that are not running, assuming the vagrant-hostsupdater plugin succeeded in removing their IPs from your /etc/hosts on vagrant halt or vagrant destroy.
I’d love some kind of easy solution for dynamic IPs for vagrant VMs.