AbstractMany coral reef fishes display remarkable genetic and phenotypic variation across their geographic ranges. Understanding how historical and contemporary processes have shaped these patterns remains a focal question in evolutionary biology since they reveal how diversity is generated and how it may respond to future environmental change. Here, we compare the population genomics and demographic histories of a commercially and ecologically important coral reef fish, the common coral grouper (Plectropomus leopardus [Lacépède 1802]), across two adjoining regions (the Great Barrier Reef; GBR, and the Coral Sea, Australia) spanning approximately 14 degrees of latitude and 9 degrees of longitude. We analysed 4548 single nucleotide polymorphism (SNP) markers across 11 sites and show that genetic connectivity between regions is low, despite their relative proximity (~100 km) and an absence of any obvious geographic barrier. Inferred demographic histories using 10,479 markers suggest that the Coral Sea population was founded by a small number of GBR individuals and that divergence occurred ~190 kya under a model of isolation with asymmetric migration. We detected population expansions in both regions, but estimates of contemporary effective population sizes were approximately 50% smaller in Coral Sea sites, which also had lower genetic diversity. Our results suggest that P. leopardus in the Coral Sea have experienced a long period of isolation that precedes the recent glacial period (~10–120 kya) and may be vulnerable to localized disturbances due to their relative reliance on local larval replenishment. While it is difficult to determine the underlying events that led to the divergence of the Coral Sea and GBR lineages, we show that even geographically proximate populations of a widely dispersed coral reef fish can have vastly different evolutionary histories.