A comparison of the equations for photosynthesis and calcification in reef corals suggests that the two processes compete for available inorganic carbon; yet reef corals exhibit simultaneous high rates of photosynthesis and calcification during daylight hours. Also, the extreme metabolic activity observed in corals at high irradiance requires a large net efflux of protons at sites of rapid calcification and respiration. Corals have resolved these problems through development of morphologies that separate the zone of rapid calcification (ZC) from the zone of rapid photosynthesis (ZP), with the fixed-carbon energy supply from the ZP being rapidly translocated to the ZC. Translocation of photosynthate from the ZP serves as a means of transporting protons to the ZC, where they are readily dissipated into the water column. Observations on the spatial relationship of the ZC and ZP, analysis of net proton flux, incorporation of photosynthate translocation coupled with an understanding of the importance of boundary layers (BL) leads to a unified hypothesis that describes the processes involved in coral metabolism. The proposed model is based on the observation that reef corals have evolved a wide range of morphologies, but all of them place the ZC between the ZP and the external seawater. This spatial arrangement places the BL in contact with the ZC in order to facilitate efflux of protons out of the corallum. Placement of the ZC between the ZP and the BL maximizes recycling of the metabolic products O2 and HCO3−. Furthermore, this arrangement maximizes the photosynthetic efficiency of zooxanthellae by producing a canopy structure with the skeletal material in the ZC serving to absorb ultraviolet radiation (UVR) while scattering photosynthetically active radiation (PAR) in a manner that maximizes absorption by the zooxanthellae. The ZP is isolated from the water column by the ZC and the BL. Therefore ZP must exchange metabolic materials with the ZC and with the water column through the ZC and its overlying BL. The resulting configuration is highly efficient and responsive to irradiance direction, irradiance intensity, water motion and coral polyp morphology. The skeletons of corals are thereby passively modified in response to physical factors such as light and water motion regime. The model presents a unified theory of coral metabolism and provides explanations for many paradoxes of coral biology, including plasticity of the diverse growth forms and an explanation for coral skeletal growth response to ocean acidification.