Summary Details on the genetics of behavioral and quantitative phenotypes remain limited to a few organisms. Such information is central to understanding both adaptation and speciation, as many of these phenotypes reduce gene flow between taxa 1–3. Hybrid zones provide an ideal arena for studying this topic, as they consist of recombinant genotypes that allow genetic mapping of traits distinguishing natural populations 4. We examined the genetic basis of migratory orientation and plumage color, both of which may contribute to speciation, in a hybrid zone between two groups of Swainson’s thrushes that differ in these traits. We identified a cluster of \SNPs\ on chromosome 4 strongly associated with migratory orientation. Genes involved with the circadian clock, nervous system, and cell signaling were located here and included candidates implicated in smaller-scale studies of migration in different animal groups, supporting previous suggestions that there is a common gene package for migration 5. Plumage color was more polygenic than migratory orientation but showed strong associations on the Z chromosome that included \SNPs\ linked to TYRP1, a gene involved in the production of eumelanin. We integrated these results with genomic data from pure populations and found that regions associated with both phenotypes co-localized with regions of elevated relative differentiation between the groups. This finding relates to the literature on islands of differentiation 6–8 by implicating divergent selection in generating these peaks. Together, our results identify specific genomic regions involved in both the regulation of complex phenotypes across animal groups and speciation 9.