We reared primary polyps (new recruits) of the common Atlantic golf ball coral Favia fragum for 8 days at 25°C in seawater with aragonite saturation states ranging from ambient (Ω = 3.71) to strongly undersaturated (Ω = 0.22). Aragonite was accreted by all corals, even those reared in strongly undersaturated seawater. However, significant delays, in both the initiation of calcification and subsequent growth of the primary corallite, occurred in corals reared in treatment tanks relative to those grown at ambient conditions. In addition, we observed progressive changes in the size, shape, orientation, and composition of the aragonite crystals used to build the skeleton. With increasing acidification, densely packed bundles of fine aragonite needles gave way to a disordered aggregate of highly faceted rhombs. The Sr/Ca ratios of the crystals, measured by SIMS ion microprobe, increased by 13%, and Mg/Ca ratios decreased by 45%. By comparing these variations in elemental ratios with results from Rayleigh fractionation calculations, we show that the observed changes in crystal morphology and composition are consistent with a >80% decrease in the amount of aragonite precipitated by the corals from each “batch” of calcifying fluid. This suggests that the saturation state of fluid within the isolated calcifying compartment, while maintained by the coral at levels well above that of the external seawater, decreased systematically and significantly as the saturation state of the external seawater decreased. The inability of the corals in acidified treatments to achieve the levels of calcifying fluid supersaturation that drive rapid crystal growth could reflect a limit in the amount of energy available for the proton pumping required for calcification. If so, then the future impact of ocean acidification on tropical coral ecosystems may depend on the ability of individuals or species to overcome this limitation and achieve the levels of calcifying fluid supersaturation required to ensure rapid growth.