Recent advances in DNA sequencing have revolutionized evolutionary biology by allowing for genome-scale studies of non-model organisms. We can now readily connect genotype with phenotype, i.e., identify the genetic basis of particular traits, a key goal in the study of evolution. In addition, genome-scale sequence analysis has shifted our understanding of the frequency and magnitude of gene flow in nature. Once viewed as important only for its role preventing divergence, the common view now is that in many taxa gene flow occurs among many lineages in the early stages of divergence. My dissertation focuses on gene flow in bearded manakins (genus Manacus), which are notable for their intense tandem courtship display, high degree of reproductive skew among males, and bright male plumage. In western Panama, yellow-collared M. vitellinus and white-collared M. candei interbreed in a narrow hybrid zone. Male vitellinus secondary sexual traits, including the yellow collar, have introgressed roughly 50 km west across the hybrid zone into candei populations and then stalled at the east bank of the Río Changuinola, the region’s largest river. Evidence from studies of male-male interaction and female choice implicate positive sexual selection for yellow collars as a driver of introgression. For thirty years since this situation was first described in detail, several key issues have remained unresolved, including why introgression has not continued across the river and what gene or genes are responsible for yellow coloration. In the first chapter, I reviewed the current state of knowledge of the Manacus hybrid zone system and proposed new hypotheses for some of the patterns exhibited by these populations. In the second chapter, I used reduced-representation genome sequencing to investigate whether reduced gene flow across the Río Changuinola alone can explain stalled trait introgression. I found that, although advantageous plumage traits have not introgressed far beyond the river, substantial gene flow is occurring, implicating an additional selective force or forces in preventing trait introgression. In the third chapter, I used whole-genome sequencing of all major Manacus lineages, including unpigmented M. manacus and pigmented M. aurantiacus, to explore the evolution and genetic basis of collar coloration. I identified the carotenoid metabolism gene beta-carotene oxygenase 2 (BCO2) as responsible for collar color differences between vitellinus and candei and uncovered evidence of past introgression introducing aurantiacus BCO2 alleles into vitellinus. I argue that gene flow is likely to be a more common mechanism than previously appreciated for spreading sexual traits among species.