Marine macroinvertebrates support important fisheries throughout the Indo-Pacific, but stocks of species such as trochus (Rochia nilotica) are easily overharvested. In north-western Australia, trochus are taken from inshore reefs by Indigenous Australians and oceanic reefs by artisanal Indonesian fishers. The management of these environmentally distinct regions relies on understanding their spatial interdependencies, yet connectivity between them has not been evaluated empirically. Here, we used genotype-by-sequencing analysis of 514 trochus samples collected from 17 locations (15 in the inshore Kimberley, 2 offshore oceanic sites). Analysis of 5428 polymorphic single nucleotide polymorphism loci revealed significant genetic subdivision between the oceanic and coastal sites, and a subset of loci exhibited significantly higher subdivision, suggesting they are subject to directional selection. Population differentiation was also evident between the two oceanic sites, but not between coastal sites. Trochus populations from the coastal Kimberley and oceanic reefs represent two genetically and demographically independent units, with preliminary evidence for local adaptation to these distinctive environments. Management strategies for R. nilotica reflect these divisions, but the limited connectivity among oceanic populations indicates that they are vulnerable to overexploitation. Furthermore, their potential adaptive distinctiveness indicates that coastal stocks may be unsuitable for replenishing oceanic stocks.