The presence of endogenous viral elements in host genomes hints towards much older host-virus relationships than predicted by exogenous phylogenies, with highly mutable single-stranded DNA (ssDNA) viruses and RNA viruses often occupying entangled multispecies ecological niches. The difficulty lies in unravelling the long-term evolutionary history of vertebrate virus-host relationships and determining the age of a potentially ancient tree based only fresh shoots at the tips. Resolving such lineages, and the sometimes great discrepancy amongst evolutionary timescales, is problematic, especially when purifying selection or recombination can significantly alter the accuracy of phylogenetic reconstruction methods. Pathogens which occupy entangled multispecies ecological niches add a further layer of complexity but we show that multi-host scenarios may also provide opportunities to identify allopatric or sympatric paleobiological signals that can unlock longer term phylogenies. We identified host-based, cryptic, sympatric differentiation in beak and feather disease virus in the Psittaciformes tribe Loriini along with endogenous circovirus motifs in Kea (Nestor notabilis) and Gondwanan vicariance estimates to infer the evolutionary timescale of the circoviruses. This demonstrated a chronology of psittacine circovirus speciation aligned to conservative Zealandic divergences for relic circovirus motifs in Kea and a 10 million year divergence coinciding with the Papuan central range orogeny that triggered the radiation of Loriini and segregation of an antecedent viral clade in Australian lorikeets. Estimates of circovirus speciation in birds highlighted a Gondwanan dominant group in Neoaves with passerine, columbid and larid circoviruses deeply separated from those in waterfowl, consistent with a Triassic divergence of Galloanserae. The circovirus tree had a deep ancestry in invertebrates with a Palaeozoic expansion in fish and mammals. We show that longer term evolutionary relationships in viruses which have a high rate of mutation and admixture can be disentangled, highlighting that contemporary virus host-switching can be explained by deep intra-lineage host phylogeny.