Visual preferences are important drivers of mate choice and sexual selection, but little is known of how they evolve at the genetic level. In this study, we took advantage of the diversity of bright warning patterns displayed by
Heliconius
butterflies, which are also used during mate choice. Combining behavioral, population genomic, and expression analyses, we show that two
Heliconius
species have evolved the same preferences for red patterns by exchanging genetic material through hybridization. Neural expression of
regucalcin1
correlates with visual preference across populations, and disruption of
regucalcin1
with CRISPR-Cas9 impairs courtship toward conspecific females, providing a direct link between gene and behavior. Our results support a role for hybridization during behavioral evolution and show how visually guided behaviors contributing to adaptation and speciation are encoded within the genome.