John,
I'll take a shot at helping but would defer to Unman who has helped me out a 
lot, both directly and indirectly on this forum.

Some notes:
Been using 3.2 and 4.0 only...haven't tried 4.0.1
No an expert but have having been hacking my way thru Qubes to make it my 
primary

I loaded 4.0, however during the setup I did not add the default whonix 
template(v13 I think) to my system as the default whonix needs to be removed in 
order to upgrade to 14. This option is chosen when loading Qubes for the first 
time.

I immediately update Dom0 using a VPN connection thru my network

After installing Qubes 4.0, I immediately install whonix-14 following these 
instructions: https://www.whonix.org/wiki/Qubes/Install

All updates going forward are done thru whonix-14-GW.........

When you say upgrading Firefox are you just updating Firefox or the whole 
template...I don't just upgrade Firefox, I update the whole template i.e. I 
update Debian and Fedora and this updates Firefox in the template and the 
appvm's associated with the template. Make sure you are aware of the 
template/appvm relationship...you don't update the appvm(e.g. sys-whonix), you 
update the template(whonix-gw) which is the source for the appvm(sys-whonix).

Other best practices I follow:
*Fresh templates seems to be the advice(vs upgrading)
*Whonix-gw is a key template to update as all my updates are done thru this 
template/appvms
* Get a VPN appvm setup as a priority
* Clone you templates and experiment on the clones, this way you can resort 
back to your clean template WHEN you F%$# it up (Not IF...you will at some 
point mess  one up)

Good luck, hope this helps... 

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