Many studies have linked genetic variation to behavior, but few connect to the intervening neural circuits that underlie the arc from sensation to action. Here, we used a combination of genome-wide association (GWA), developmental gene expression, and photoreceptor electrophysiology to investigate the architecture of mate choice behavior in Heliconius cydno butterflies, a clade where males identify preferred mates based on wing color patterns. We first found that the GWA variants most strongly associated with male mate choice were tightly linked to the gene controlling wing color in the K locus, consistent with previous mapping efforts. RNA-seq across developmental time points then showed that seven genes near the top GWA peaks were differentially expressed in the eyes, optic lobes, or central brain of white and yellow H. cydno males, many of which have known functions in the development and maintenance of synaptic connections. In the visual system of these butterflies, we identified a striking physiological difference between yellow and white males that could provide an evolutionarily labile circuit motif in the eye to rapidly switch behavioral preference. Using single-cell electrophysiology recordings, we found that some ultraviolet (UV)-sensitive photoreceptors receive inhibition from long-wavelength photoreceptors in the male eye. Surprisingly, the proportion of inhibited UV photoreceptors was strongly correlated with male wing color, suggesting a difference in the early stages of visual processing that could plausibly influence courtship decisions. We discuss potential links between candidate genes and this physiological signature, and suggest future avenues for experimental work. Taken together, our results support the idea that alterations to the evolutionarily labile peripheral nervous system, driven by genetic and gene expression differences, can significantly and rapidly alter essential behaviors.