Circovirus phylogeny parallels host phylogeny with early host-switching between avian and mammalian viruses.
High mutation signals in contemporary viruses can grossly underestimate evolutionary timescales.
Emphasises Australia and New Guinea as an evolutionary hotspot for avian circovirus evolution.
Highlights the cryptic effects of population genetic structure, selection pressure and recombination on phylogeny.
We demonstrate a deep host-history phylogenetic basis for contemporaneous virus host-switching.