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Oceanic absorption of atmospheric CO2 results in alterations of carbonate chemistry, a process coined ocean acidification (OA). The economically and ecologically important eastern oyster (Crassostrea virginica) is vulnerable to these changes because low pH hampers CaCO3 precipitation needed for shell formation. Organisms have a range of physiological mechanisms to cope with altered carbonate chemistry; however, these processes can be energetically expensive and necessitate energy reallocation. Here, the hypothesis that resilience to low pH is related to energy resources was tested. In laboratory experiments, oysters were reared or maintained at ambient (400 ppm) and elevated (1300 ppm) pCO2 levels during larval and adult stages, respectively, before the effect of acidification on metabolism was evaluated. Results showed that oysters exposed to elevated pCO2 had significantly greater respiration. Subsequent experiments evaluated if food abundance influences oyster response to elevated pCO2. Under high food and elevated pCO2 conditions, oysters had less mortality and grew larger, suggesting that food can offset adverse impacts of elevated pCO2, while low food exacerbates the negative effects. Results also demonstrated that OA induced an increase in oyster ability to select their food particles, likely representing an adaptive strategy to enhance energy gains. While oysters appeared to have mechanisms conferring resilience to elevated pCO2, these came at the cost of depleting energy stores, which can limit the available energy for other physiological processes. Taken together, these results show that resilience to OA is at least partially dependent on energy availability, and oysters can enhance their tolerance to adverse conditions under optimal feeding regimes.