The invasive ectoparasite Sarcoptes scabiei affects the welfare and conservation of Australian marsupials. Molecular data suggest that spillover from other hosts may be responsible for the emergence of this infectious disease, but the scale of such studies is limited. We performed expanded molecular typing of the S. scabiei mitochondrial cox1 gene from 81 skin scrapings from infested wombats (Vombatus ursinus), koalas (Phascolarctos cinereus), red foxes (Vulpes vulpes), and dogs (Canis lupus familiaris) across Australia. Combined with existing S. scabiei sequences, our analysis revealed 16 haplotypes among Australian animals, sharing between 93.3% and 99.7% sequence similarity. While some sequences were unique to specific hosts or to Australia, key haplotypes could be detected across several marsupial hosts as well as to wild or domestic canids in Australia. We identified 43 cox1 haplotypes with many Australian haplotypes identical to S. scabiei mites from inside and outside Europe. We concluded that multiple introduction events were plausible explanations to the origin and emergence of this parasite into Australian marsupials and that disease spillover from canids was likely. Together, our greatly expanded S. scabiei sequence dataset provided a more nuanced picture of both spillover and sustained intraspecific transmission for this important parasite.