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The Oriental fruit flyBactrocera dorsalis(Hendel), a global pest that can decimate regional fruit industries and elicit international quarantines, has been the subject of considerable taxonomic confusion. Previous phylogenetic work revealed thatB. dorsalisis part of a monophyletic clade containing 12 species. We present restriction site‐associated DNA sequencing (RAD‐seq) genomic data for 2,292 specimens, which unequivocally supports the delimitation of two new species, here described asBactrocera borneoensissp. n.Doorenweerd & San Jose andB. incognitasp. n.Doorenweerd & San Jose. We additionally obtained 1,985 Cytochrome C oxidase I (COI) sequences for a subset of the specimens to see which species can be diagnosed with this mtDNA marker and conclude thatB. dorsalis,B. incognita,B. carambolaeDrew & Hancock,B. raiensisDrew & Hancock,B. occipitalis(Bezzi) andB. kandiensisDrew & Hancock cannot be identified reliably using COI due to introgression—but the newly described speciesB. borneoensiscan be identified using COI. The supposed innocuous speciesB. raiensisdistribution is underestimated in Asia and Africa.Bactrocera kandiensisCOI genotypes occur in African flies, but RAD‐seq data confirm that these areB. dorsaliswith introgressedB. kandiensisCOI. The phylogenomic dataset brings new light to the extent of theB. dorsalis s.l.clade and the morphological and molecular confusion based on COI. This will have ramifications for ecological data—including host and distribution ranges—associated withB. dorsalis s.l.clade species, pest identification protocols and our understanding of the economic importance of the various species in the clade.