The effective management of a coral reef system relies on a detailed understanding of the population structure of dominant habitat-forming species. For some corals, however, high levels of phenotypic plasticity have made species delineation based on morphological characteristics alone unreliable, suggesting that previous studies of population genetic structure may have been influenced by the inclusion of multiple genetic lineages in the analyses. We examined the population structure of the Pocillopora damicornis morphospecies along the World Heritage Ningaloo Coast, Western Australia, and recovered 2 mitochondrial haplotypes from sympatrically occurring colonies possessing morphological characteristics consistent with taxonomic classification of P. damicornis. Despite a high degree of genetic differentiation between these lineages, we detected low levels of unidirectional admixture between them, suggesting that reproductive barriers are not fully developed. We found dual modes of reproduction for both lineages with considerable variation in the contribution of sexual reproduction among sample sites. Lastly, we identified a high dispersal potential of sexually produced propagules in the most common lineage with positive spatial autocorrelation detected over distances up to 60 km. Based on these results, it appears that populations of P. damicornis have a high capacity to recover from environmental perturbations as long as the effects of disturbances are patchy across Ningaloo Reef.