Local variation in microclimate, with extreme events amplified by ongoing climate change, can drive divergent physiological responses to warming across populations. As habitat temperature characteristics shift with climate change, populations may be required to use plasticity to deal with rapid shifts in thermal extremes. Applying a population genomics approach (RADseq), we investigated heat tolerance and metabolic rate in the direct-developing sea hare, Phyllaplysia taylori, to determine whether short-term plasticity was influenced by differences in microclimate. Using this method, we identified possible correlations between thermal tolerance phenotype and genotype in P. taylori collected from sites along the western US coast from Ocean Shores, WA to Morro Bay, CA, that were acclimated to winter, summer, and future summer temperatures. P. taylori from all locations consistently exhibited critical thermal maxima (CT_max) above habitat temperatures, even when average daily variation in habitat temperature was considered (CT_max ranged from 24-35ºC, average=30.1±0.2ºC; average habitat temperature ranged from 12-20ºC, average=21±0.8ºC). CT_max and compensatory metabolic suppression after heat stress were correlated to habitat temperature, whereas only metabolic suppression was correlated with genetic structure. The breadth of plastic responses we observed (11ºC) was substantially wider than reported for other poikilothermic taxa in the literature and did not appear to be population-specific. Our findings suggest that high plasticity of thermal tolerance precedes local adaptation, and improves the physiological resilience of populations under climate change.