The semienclosed Bouraké lagoon in New Caledonia is a natural system that enables observation of evolution in action with respect to stress tolerance in marine organisms, a topic directly relevant to understanding the consequences of global climate change. Corals inhabiting the Bouraké lagoon endure extreme conditions of elevated temperature (> 33°C), acidification (7.2 pH units), and deoxygenation (2.28 mg O2 L-1), which fluctuate with the tide due to the lagoon's geomorphology. To investigate the underlying bases of the apparent stress tolerance of these corals, we combined whole genome resequencing of the coral host and ITS2 metabarcoding of the photosymbionts from 90 Acropora tenuis colonies from three localities along the steep environmental gradient from Bouraké to two nearby control reefs. Our results highlight the importance of coral flexibility to associate with different photosymbionts in facilitating stress tolerance of the holobiont; but, perhaps more significantly, strong selective effects were detected at specific loci in the host genome. Fifty-seven genes contained SNPs highly associated with the extreme environment of Bouraké and were enriched in functions related to sphingolipid metabolism. Within these genes, the conserved sensor of noxious stimuli TRPA1 and the ABCC4 transporter stood out due to the high number of environmentally selected SNPs that they contained. Protein 3D structure predictions suggest that a single-point mutation causes the rotation of the main regulatory domain of TRPA1, which may be behind this case of natural selection through environmental filtering. While the corals of the Bouraké lagoon provide a striking example of rapid adaptation to extreme conditions, overall, our results highlight the need to preserve the current standing genetic variation of coral populations to safeguard their adaptive potential to ongoing rapid environmental change.