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Abstract Animal genitalia evolve rapidly because of coevolution between male and female traits. However, how the ecological context in which mating occurs might modulate the evolution of genital traits remains poorly understood. We investigated how a change in the sensory environment (the absence of light upon cave colonization) impacted the expression of genital traits in a live-bearing fish, Poecilia mexicana (Poeciliidae), with populations in adjacent cave and surface habitats. Quantifying characteristics of the female urogenital aperture and the male gonopodium (a modified anal fin used for copulation), we found significant differences in genital traits of both sexes. Females from cave populations exhibited larger and more rounded genitalia. Males from cave populations exhibited a significantly enlarged palp, a fleshy gonopodial appendage that has been hypothesized to have sensory functions. Our results suggest that genital traits can diverge rapidly among closely related populations exposed to different environmental conditions. The absence of light could impact genital evolution directly, if some genital structures have sensory functions that compensate for the lack of visual information during copulation, or indirectly, if the absence of light impacts dynamics of sexual conflict or cryptic female choice that arise through the interaction between the sexes.