Climate change challenges organismal fitness by creating a mismatch between phenotypes based on historic conditions and the new environment. Rapid compensatory response to environmental change, or adaptive phenotypic plasticity generated by epigenetic mechanisms (e.g., DNA methylation) can provide a temporal buffer for evolution through natural selection, and may therefore be especially crucial for sessile marine organisms, such as reef-building corals. We tested the potential for scleractinian corals to exhibit phenotypic plasticity and altered DNA methylation in response to ocean acidification (OA). Clonal fragments of the environmentally susceptible coral Pocillopora damicornis and environmentally resistant Montipora capitata were exposed to ambient pH (7.9-7.65) and low pH (7.6-7.35) conditions in common garden tanks at ambient temperature (26.6°C) for ~6 weeks. Response was assessed by growth as a proxy for fitness, 1H-NMR profiling or physiological phenotype, and host DNA methylation as a measure of epigenetic change. M. capitata responded weakly to OA, with no difference in growth, minimal separation of metabolite profiles, and no change in DNA methylation between treatments. Conversely, P. damicornis exhibited a significant decline in growth (30%) at low pH, stronger separation in metabolite profiles between the two treatments, and a higher DNA methylation (~2x) at low pH than ambient. Our results suggest some corals have a more sensitive environmental trigger for real-time epigenetic reprogramming and provide evidence of a mechanism whereby intra-generational and trans-generational acclimatization and soft inheritance may occur, which has significant implications for future reef persistence.