In mosaic marine habitats, such as intertidal zones, ocean acidification (OA) is exacerbated by high variability of pH, temperature, and biological CO2 production. The nonlinear interactions among these drivers can be context-specific and their effect on organisms in these habitats remains largely unknown, warranting further investigation. We were particularly interested in Mytilus edulis (the blue mussel) from intertidal zones of the Gulf of Maine (GOM), USA, for this study. GOM is a hot spot of global climate change (average sea surface temperature (SST) increasing by >0.2°C/year) with >60% decline in mussel population over the past 40 years. Here, we utilize bioenergetic underpinnings to identify limits of stress tolerance in M. edulis from GOM exposed to warming and OA. We have measured whole-organism oxygen consumption rates and metabolic biomarkers in mussels exposed to control and elevated temperatures (10 vs. 15°C, respectively) and current and moderately elevated PCO2 levels (~400 vs. 800 µatm, respectively). Our study demonstrates that adult M. edulis from GOM are metabolically resilient to the moderate OA scenario but responsive to warming as seen in changes in metabolic rate, energy reserves (total lipids), metabolite profiles (glucose and osmolyte dimethyl amine), and enzyme activities (carbonic anhydrase and calcium ATPase). Our results are in agreement with recent literature that OA scenarios for the next 100–300 years do not affect this species, possibly as a consequence of maintaining its in vivo acid-base balance.