Several millennia of human-mediated translocation of non-native pig species (genus Sus) to the islands of Wallacea and Oceania have considerably altered local ecosystems. To investigate the timing and trajectory of these introductions, we conducted both genomic analyses of 576 pig nuclear genomes and a geometric morphometric analysis of 708 modern and ancient dental remains. Our analyses demonstrate that free-living and domestic pigs in Wallacea and Oceania have diverse ancestries resulting from the introduction of multiple sequential pig populations followed by gene flow. Despite the variability in their genomic ancestry, these pigs all have a distinct tooth morphology as well as a genetic link to the Chinese domestic pig populations that accompanied the dispersal of Austronesian language speakers ~4000 to 3000 years ago via Taiwan and the Philippines.