Because of their widespread agricultural impact and rapid range expansions, true fruit flies (Tephritidae) are the subject of quarantine and control efforts worldwide. Among these flies, the pumpkin fruit fly Bactrocera depressa, which infests squash and other cucurbitaceous plants in Korea, Japan and Taiwan, was recently isolated from produce shipments entering Japan and identified as a regulatory target. This species was described in 1933 from collections in Japan and discovered in 1974 in Korea, suggesting that it may have recently invaded mainland Asia. We analysed the genetic structure of Asian populations of B. depressa using sequence variation for mitochondrial gene cytochrome-oxidase I and three nuclear loci: elongation factor 1α, tubulinβ1 and tubulinβ3, using frequency-based approaches, nested clade analysis and assignment tests. Contrary to the hypothesis of recent invasion, high levels of genetic subdivision were found among five Korean and three Japanese populations. Nested clade analysis suggested a variety of processes operating over different time scales, including ancient isolation between Korea and Japan and more recent range expansions within each country. Contrary to a priori expectations, the results also suggested the recent introduction of a mitochondrial haplotype into Yokohama, Japan that is related closely to a widespread haplotype found throughout Korea. Assignment tests also supported these conclusions. The combination of a genealogical approach and probabilistic assignments of individuals to populations of origin was able to provide statistical support for the identification of cryptic introductions within an otherwise widespread indigenous species.