Australia and Southeast Asia are hotspots of global diversity in the fruit-fly genus Bactrocera. Although a great diversity of species has been long recognised, evolutionary relationships are poorly understood, largely because previous sequencing techniques have provided insufficient historical signal for phylogenetic reconstruction. Poorly understood biogeographic history in Bactrocera has prevented a deeper understanding of migratory patterns in this economically important pest group. Using representatives from Australia and Malaysia, we tested the utility of a genome-reduction approach that generates thousands of single-nucleotide polymorphisms for phylogenetic reconstructions. This approach has high utility for species identification because of the ease of sample addition over time, and the species-level specificity able to be achieved with the markers. These data have provided a strongly supported phylogenetic tree congruent with topologies generated using more intensive sequencing approaches. In addition, our results do not support taxonomic assignments to species complex for a number of species, such as B. endiandrae in the dorsalis complex, yet find a close relationship between B. pallida and the dorsalis species. Our data have further validated non-monophyletic evolution of male response to primary attractants. We also showed at least two diversification events between Australia and Southeast Asia, indicating trans-regional dispersal in important pest species.