Evolutionary relationships in the black-lip pearl oyster Pinctada margaritifera which is highly valued for pearl production remain poorly understood. This species possesses an 18,000 km Indo-Pacific natural distribution, and its current description includes six subspecies defined exclusively on morphological characters. To evaluate its taxonomic identity using molecular data, 14 populations in both the Indian and Pacific Oceans (n = 69), and the congeneric taxa P. maxima and P. mazatlanica (n = 29 and n = 10, respectively) were sampled. Phylogenomic reconstruction was carried out using both 8,308 genome-wide SNPs and 10,000 dominant loci (DArTseq PAVs). Reconstructions using neighbour-joining (Nei's 1972 distances), maximum likelihood and Bayesian approaches all indicate that the taxonomy of P. margaritifera is quite complex, with distinct evolutionary significant units (ESUs) identified within Tanzanian and Iranian populations. Contrastingly, phylogenies generated for Pacific Ocean oysters resolved a large monophyletic clade, suggesting little support for two current morphological subspecies classifications. Furthermore, P. mazatlanica formed a basal clade closest to French Polynesian P. margaritifera, suggesting it may be conspecific. Collectively, these findings provide evidence that P. margaritifera comprises a species complex, perhaps as a result of population fragmentation and increased divergence at range limits.