Slowing coral reef degradation under rapid climate change requires conservation strategies that apply larval connectivity and genetic diversity patterns to processes of recovery and adaptation. Coral metapopulations are thought to be sustained by self-recruitment, with recovery and adaptation supplemented by the exchange of beneficial genes from distant populations, but little evidence is available to substantiate this hypothesis. Here, we used genotype data to measure the distribution of genomic diversity of brooding coral Isopora brueggemanni across northwest Australia (NWA). Parentage analysis revealed high rates of self-recruitment (>30%) to local reef patches, providing direct evidence that coral population replenishment is driven by local production. Furthermore, a distinct genomic diversity structure could be observed across NWA. We also found evidence of distinct lineages, adapted to fine-scale environmental conditions, living in sympatry at Scott reefs, indicating processes other than self-recruitment influence genomic diversity. Even though, high level of local genetic diversity persisted through multiple disturbances at Scott reefs, benefiting longer-term population adaptability and recovery, ongoing population maintenance will still rely on sufficient surviving broodstock, and connectivity networks that match larval dispersal patterns. Hence, re-evaluating future trajectory of brooding corals is crucial, especially when the severity of impacts is likely to increase in the future.