The leafscale gulper (Centrophorus squamosus) is a wide-ranging deepwater benthopelagic shark threatened by commercial fisheries in parts of its range. Despite concerns about resource sustainability, little is known about the population structure and connectivity between critical habitats of the leafscale gulper. This study investigates the genetic population structure and the migration patterns of C. squamosus using nuclear microsatellites and mitochondrial NADH dehydrogenase subunit 2 (ND2) gene sequences. Genetic diversity was estimated and compared among sample collections from off Ireland, Portugal, the Azores, South Africa and New Zealand. The null hypothesis of genetic homogeneity among all collections was not rejected by the nuclear loci (FST (the overall genetic differentiation among sample collections) = –0.002, P = 0.88), but we found long-term genetic divergence between New Zealand and the remaining collections at the mtDNA ND2 (FCT (genetic differentation among groups of sample collections) = 0.366, P = 0.000). Migration rate estimates indicated limited female dispersal across the Indian Ocean whereas males showed less restricted dispersal. Our results are consistent with a single genetic stock of C. squamosus and the existence of sex-biased dispersal across the Indian Ocean. Widespread genetic homogeneity at nuclear loci minimizes the loss of unique adaptive genetic diversity in the event of localised depletion. However, high local fishing mortality may have far reaching impacts given the marked sex- and maturity-stage-based habitat partitioning previously reported for C. squamosus.