Upstream colonisations from islands to continents have played an important role in the evolution of at least two major global bird radiations – the oscine passerines and the pigeons. Here we investigate the dynamics of insular diversification and upstream dispersal of pigeons(Columbiformes) within the Indo-Australian Archipelago. Based on a supermatrix fossil-calibrated phylogeny and model-based biogeographic analyses islands of Melanesia, now centred on New Guinea and considered separately from Australia, have been centre of pigeon diversification since the Eocene-Oligocene transition (~ 34 Ma). Geological reconstructions are concordant in suggesting arc terranes and continental ribbon fragments that underpin the contemporary Melanesian region may have formed extensive archipelagos separate from the main Australian landmass for much of the Oligocene and Miocene. For most of the last 35 million years these islands are inferred to have functioned as a net source of pigeon lineages for Asia, and especially Australia. However, the probability and evolutionary outcomes of upstream colonisation vary greatly across lineages and regions. Arboreal fruit-eating pigeons have colonised nearby continents on multiple occasions yet show little evidence of subsequent radiation. In contrast, insular terrestrial pigeons have been largely unable to colonise Asia, while a single early colonisation of Australia preceded an endemic radiation.