Most studies on coral reefs have focused on shallow reef (<30 m) systems due to the technical limitations of conducting scientific diving deeper than 30 m. Compared to their shallow-water counterparts, these mesophotic coral reefs (30–150 m) are understudied, which has slowed our broader understanding of the biodiversity, ecology, and connectivity of shallow and deep coral reef communities. We know that the light environment is an important component of the productivity, physiology, and ecology of corals, and it restricts the distribution of most species of coral to depths of 60 m or less. In the Bahamas, the coral Montastraea cavernosa has a wide depth distribution, and it is one of the most numerous corals at mesophotic depths. Using a range of optical, physiological, and biochemical approaches, the relative dependence on autotrophy vs. heterotrophy was assessed for this coral from 3 to 91 m. These measurements show that the quantum yield of PSII fluorescence increases significantly with depth for M. cavernosa while gross primary productivity decreases with depth. Both morphological and physiological photoacclimatization occurs to a depth of 91 m, and stable isotope data of the host tissues, symbionts, and skeleton reveal a marked decrease in productivity and a sharp transition to heterotrophy between 45 and 61 m. Below these depths, significant changes in the genetic composition of the zooxanthellae community, including genotypes not previously observed, occur and suggest that there is strong selection for zooxanthellae that are suited for survival in the light-limited environment where mesophotic M. cavernosa are occurring.