Sexual selection produces some of the most extraordinary traits and behaviors found in nature and is believed to play a key role in speciation, yet the underlying genomics are not well understood. We analyzed the genomic consequences of sexual selection underlying asymmetric introgression in male secondary sexual traits across an avian hybrid zone. Where Manacus candei (white-collared manakin) and M. vitellinus (golden-collared manakin) come into contact in northwestern Panama, plumage color and behavioral traits of male M. vitellinus have introgressed under sexual selection into Manacus candei , producing populations that look and act like vitellinus but are genetically like candei . We show that the introgressing plumage traits are due to deposition of lutein and melanin pigments in collar and belly feathers, respectively. To determine the genetic basis of these traits, we resequenced genomes from two Manacus candei-like populations, one with golden collars and one with white, and from one M. vitellinus population. Comparison of these populations identified divergent genomic regions containing genes involved in carotenoid metabolism and melanization, and implicates additional signaling pathways that may be involved in feather development and gonadotropin expression. These findings provide a novel example of genomic targets and mechanisms regulating expression of secondary sexual traits.