Climate change threatens the survival of coral reefs globally, primarily through mass bleaching and mortality as a result of marine heatwave events. While these short-term effects are clear, predicting the fate of coral reefs over the coming century is a major challenge. One way to understand the longer-term effects of rapid climate change is to examine the response of coral populations to past climate shifts. Coastal and shallow-water marine ecosystems such as coral reefs have been reshaped many times by sea-level changes during the Pleistocene, yet, few studies have been able to directly link this with its consequences on population demographics, dispersal, and adaptation. Here we use whole-genome sequencing data to explore such links for the reef-building coral, Acropora digitifera, in northwestern Australia. We identify three genetically distinct populations and show that their rapid divergence since the last glacial maximum (LGM) is likely driven by founder-effects. Signatures of recent selective sweeps are present in all three populations with different patterns of functional enrichment between inshore and offshore habitats. However, the photosymbiont communities are largely undifferentiated between all three locations indicating that selection on host genes has been the primary driver of adaptation for this species in northwestern Australia.