IANAL, but had an exchange with a few lawyers on this very subject a few years back when my son turned 18.
VA is a case law state, so many things are not explicitly stated in state law but are derived from prior case decisions.
A previous VA AG provided written interpretation/opinion of the "secured in a container or compartment" section, and I've not heard of anything since then overriding that interpretation (and I try to track such things). He stated that the securing device (glove box, center console, pistol case, etc.) did not need to be locked, or even lockable. But by case law, there does have to be some form of securing (clasp, latch, catch, zipper, etc.). So if your center console only flops open - no-go, but if it has even a spring-loaded catch, then good to go.
So a loaded handgun may be kept in your vehicle in VA (in legal locations - some locations are no-go such as schools with some exceptions) if you are of legal age to possess it (18 - with exceptions in certain localities based on magazine capacity due to interpretations of "assault weapons" - don't recall full restrictions on locations, etc., but some localities don't allow greater than 20-round magazines unless possessor has a CHP) as long as it is "secured" within an enclosure that has some sort of positive retention to the enclosure's access.