Genomic studies are uncovering extensive cryptic diversity within reef-building corals, suggesting that evolutionarily and ecologically relevant diversity is highly underestimated in the very organisms that structure coral reefs. Despite the essential ecological role of reef-building corals and urgent concerns about how populations will evolve in the Anthropocene, the processes shaping coral diversity are poorly understood. Here, we use low-coverage genome-wide sequencing of the reef-building coral Acropora tenuis (n=463) and associated endosymbiotic algae to investigate cryptic species diversity across the GBR. We discover three distinct and sympatric genetic clusters of coral hosts, whose distributions appear associated with latitude and inshore-offshore reef position. Demographic modelling suggests that the divergence history of three distinct host taxa ranges from 0.5 – 1.5 million years ago, preceding the GBR’s formation, and has been characterised by low ongoing inter-taxon gene flow, consistent with occasional hybridisation and introgression typifying coral evolution. Endosymbiont plastid diversity is not strongly associated with host identity but varies with reef location relative to shore, possibly reflecting local selective pressures maintaining coral holobiont differentiation. The strong influence of environment (but not host identity) on endosymbiont community composition supports the notion that endosymbiont diversity enables corals to match their habitat and may contribute to coral adaptation under future environmental change.