Even for a euryhaline invertebrate, the eastern oyster (Crassostrea virginica) inhabits an especially broad range of conditions. Its geographic range extends from the Gulf of St. Lawrence, Canada, to the Gulf of Mexico, where it inhabits estuaries with salinities ranging from 4-35 PSU, and annual water temperatures ranging from -2 degrees C to 36 degrees C. In some organisms, this kind of broad tolerance is achieved with a single ‘general purpose’ phenotype, capable of surviving all conditions, whereas in others, broad tolerance at the species level is achieved through local adaptation, where a series of populations are each optimized to their individual conditions, collectively comprising a species with broad tolerance. We tested these competing scenarios in a series of three experiments, each comparing the physiological and transcriptomic responses to a single stressor (either hypoxia, low salinity, or high temperatures) between populations of C. virginica that differed in their histories of exposure to that stressor. While a portion of the transcriptomic response to each stressor was unique to individual populations, we observed a strong signature of parallel physiological and transcriptomic responses to stress across populations. Genes involved in transcriptomic response to stress also tended to have lower Ka/Ks values, suggesting purifying selection. Taken together, our results suggest that the broad environmental range of C. virginica is achieved through a set of conserved physiological responses to environmental stress, and that these responses are largely shared across disparate populations.