Can somebody clarifies how qubes-update-check service works and how dom0 gets update notifications for TemplateVMs that are never powered on?

It is something basic but not obvious.

When you use apt-cacher-ng the repository definitions are rewritten so
that https:// becomes http://HTTPS///. This is so that the caching
proxy can see the request, and then forward it on encrypted as TLS
traffic.

When you use a template based qube, the repository definitions are
taken from the template, and so use that same http://HTTPS/// format.
Unless you have taken steps to use the caching proxy from the qube,
by setting a Proxy setting to the IP address of the cacher qube, then
your qube will try to connect directly to the repository. But the DNS
server will not recognise HTTPS/// as an address format, and will
return an error. This is why the Debian qubes do not report any
available updates: the Fedora qube, where the repository definitions have
not been rewritten, can access repositories and so will report when
updates are available.

I never presume to speak for the Qubes team.
When I comment in the Forum I speak for myself.

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