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Abstract Sensory drive can lead to the evolution of signals that are optimized to the environment in which they are perceived. However, when environmental conditions change, the interactions between signal, environment, and receiver may also shift, leading to the evolution of a new signal optimum or more categorical shifts in sexual signals (gains or losses). We evaluated how visual systems have evolved following a change in environment and male signal, and whether visual system divergence contributes to reproductive isolation between ancestral and derived types in red and black morphs of Pacific Northwest freshwater threespine stickleback. We found that opsin sequence was tuned to enhance the perceived contrast of black fish on a red-shifted light background, whereas opsin expression was not. Further, we found no evidence for homotypic preferences or assortative mating between colour morphs; males of both morphs were equally successful in no-choice mating contexts, perhaps because black males are more vigorous courters. Together, our results suggest that habitat transitions in black stickleback have led to a shift in sensory-drive dynamics with some aspects of the visual system and behaviour evolving in response to other factors (foraging or predation) or lagging behind the evolution of opsin sequences in red-shifted environments.