The contributions of temporal and spatial environmental variation to physiological variation remain poorly resolved. Rocky intertidal zone populations are subjected to thermal variation over the tidal cycle, superimposed with micro-scale variation in individuals’ body temperatures. Using the sea mussel (Mytilus californianus), we assessed the consequences of this micro-scale environmental variation for physiological variation among individuals, first by examining the latter in field-acclimatized animals, second by abolishing micro-scale environmental variation via common garden acclimation, and third by restoring this variation using a reciprocal outplant approach. Common garden acclimation reduced the magnitude of variation in tissue-level antioxidant capacities by ~30% among mussels from a wave-protected (warm) site, but it had no effect on antioxidant variation among mussels from a wave-exposed (cool) site. The field-acclimatized level of antioxidant variation was restored only when protected-site mussels were outplanted to a high, thermally stressful site. Variation in organismal oxygen consumption rates reflected antioxidant patterns, decreasing dramatically among protected-site mussels after common gardening. These results suggest a highly plastic relationship between individuals’ genotypes and their physiological phenotypes that depends on recent environmental experience. Corresponding context-dependent changes in the physiological mean-variance relationships within populations complicate prediction of responses to shifts in environmental variability that are anticipated with global change.