One of the main challenges in coral reef conservation and restoration is the identification of coral populations resilient under global warming. Seascape genomics is a powerful tool to uncover genetic markers potentially involved in heat tolerance among large populations without prior information on phenotypes. Here, we aimed to confirm the role of several candidate heat associated loci identified using this method in driving the phenotypic response of Acropora millepora from New Caledonia to thermal stress. We subjected 7 colonies to a long-term ex-situ heat stress assay (4°C above the Maximum Monthly Mean) and investigated their physiological response along with their Symbiodiniaceae communities and genotypes. Despite having similar thermal histories and associated symbionts, these conspecific individuals differed greatly in their tolerance to heat stress. More importantly, the clustering of individuals based on their alleles at the candidate loci was able to resolve most of the phenotypic variation in heat tolerance. Colonies harboring a higher proportion of beneficial alleles sustained on average lower mortality, higher Symbiodiniaceae/chlorophyll concentrations and photosynthetic efficiency under prolonged heat stress. Together these results support the relevance of seascape genomics to reveal candidate loci for heat adaptation in corals and develop predictive models of heat tolerance.