Torque teno virus (TTV) is a non-enveloped single-stranded, negative sense DNA virus and a major component of non-pathogenic virobiota of humans, non-human primates, and some farm animals. In recent years, pigeon associated TTV (PTTV) has been identified and genetically characterised in different parts of the world, although the breadth of genetic diversity, epidemiology or phylogenetic structure of PTTV is yet to be explored. We tested 139 pigeons from 22 endemic Columbid species from Australia, Papua New Guinea and New Zealand and identified PTTV with very high frequency (98%). Downstream phylogenetic analyses using complete genome as well putative capsid protein sequences unveiled several well supported lineage that vastly expanded the known diversity in PTTV and provided evidence for deep host codivergence. The population genetic structure of PTTV lacked significant spatiotemporal signal but demonstrated cryptic gene flow among different host adapted clusters highlighting frequent host-switching events. Our calibrated tree topology shows major divergences in PTTV amongst old world pigeon that coincided with palaeobiological events of Papuan uplift in the Early- to Mid-Miocene era.