Analyses of genetic diversity can shed light on both the origins of biodiversity hotspots, as well as the conservation status of species that are impacted by human activities. With these objectives, we assembled a genomic dataset of 14,935 single nucleotide polymorphisms from 513 grey reef sharks (Carcharhinus amblyrhynchos) sampled across 17 locations in the tropical Indo-Pacific. We analysed geographic variation in genetic diversity, estimated ancient and contemporary effective population size (N-e) across sampling locations (using coalescent and linkage disequilibrium methods) and modelled the history of gene flow between the Coral Triangle and the Coral Sea. Genetic diversity decreased with distance away from the Coral Triangle and north-western Australia, implying that C. amblyrhynchos may have originated in this region. Increases in N-e were detected across almost all sampling locations 40,000-90,000 generations ago (approximately 0.6-1.5 mya, given an estimated generation time of 16.4 years), suggesting a range expansion around this time. More recent, secondary increases in N-e were inferred for the Misool and North Great Barrier Reef sampling locations, but joint modelling did not clarify whether these were due to population growth, migration, or both. Despite the greater genetic diversity and ancient N-e observed at sites around Australia and the Coral Triangle, remote reefs around north-western New Caledonia had the highest contemporary N-e, demonstrating the importance of using multiple population size assessment methods. This study provides insight into both the past and present demographics of C. amblyrhynchos and contributes to our understanding of evolution in marine biodiversity hotspots.