Coral persistence in the Anthropocene depends on interactions among holobiont partners (coral animals and microbial symbionts) and their environment. Cryptic coral lineages-genetically distinct yet morphologically similar groups-are critically important as they often exhibit functional diversity relevant to thermal tolerance. In addition, environmental parameters such as thermal variability may promote tolerance, but how variability interacts with holobiont partners to shape responses to thermal challenge remains unclear. Here, we identified three cryptic lineages of Siderastrea siderea in Bocas del Toro, Panamá that differ in distributions across inshore and offshore reefs, microbial associations, phenotypic traits of holobiont partners (i.e., phenomes), and skeleton morphologies. A thermal variability experiment failed to increase thermal tolerance, but subsequent thermal challenge and recovery revealed that one lineage maintained elevated energetic reserves, photochemical efficiency, and growth. Last, coral cores highlighted that this lineage also exhibited greater growth historically. Functional variation among cryptic lineages highlights their importance in predicting coral reef responses to climate change.