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Anthropogenic influences on global processes and climatic conditions are increasingly affecting ecosystems throughout the world. Hawaii Island's native ecosystems are well studied and local long-term climatic trends well documented, making these ecosystems ideal for evaluating how native taxa may respond to a warming environment. This study documents adaptive divergence of populations of a Hawaiian picture-winged Drosophila, D. sproati, that are separated by only 7 km and 365 m in elevation. Representative laboratory populations show divergent behavioral and physiological responses to an experimental low-intensity increase in ambient temperature during maturation. The significant interaction of source population by temperature treatment for behavioral and physiological measurements indicates differential adaptation to temperature for the two populations. Significant differences in gene expression among males were mostly explained by the source population, with eleven genes in males also showing a significant interaction of source population by temperature treatment. The combined behavior, physiology, and gene expression differences between populations illustrate the potential for local adaptation to occur over a fine spatial scale and exemplify nuanced response to climate change.