Browser toolbox preferences have some strange semantics. The first time the browser toolbox is opened (on a machine I think, but maybe for a given profile), a new profile is created for the toolbox and the currently profile's preferences are copied over to it. When the browser toolbox is opened at later times, its preferences are left unchanged. This is problematic for several reasons:
It's pretty confusing when the browser toolbox is opened and its behavior doesn't match up with the original firefox instance's preferences.
There isn't an easy way to change the browser toolbox preferences. On macOS I have to right click the toolbox process in the dock, select "New Window", then go to about:config in that new window to modify the prefs.
This allows mochitests to interact with each other. If several mochitests in a test run try to open the browser toolbox with different sets of preferences, the toolbox will only use the preferences from the first test which opened the toolbox. This is preventing bug 1444064 from landing.
The best thing to do here is I think to always copy over the current profile's preferences to the browser toolbox profile when opening the browser toolbox. This is easy to do and addresses all of the above points.