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Abstract Seasonal migration has fascinated scientists and natural historians for centuries. While the genetic basis of migration has been widely studied across different taxa, there is little consensus regarding which genomic regions play a role in the ability to migrate and whether they are similar across species. Here, we examine the genetic basis of intraspecific variation within and between distinct migratory phenotypes in a songbird. We focus on the Common Yellowthroat (Geothlypis trichas) as a model system because the polyphyletic origin of eastern and western clades across North America provides a strong framework for understanding the extent to which there has been parallel or convergent evolution in the genes associated with migratory behavior. First, we investigate genome-wide population genetic structure in the Common Yellowthroat in 196 individuals collected from 22 locations across breeding range. Then, to identify candidate genes involved in seasonal migration, we identify signals of putative selection in replicate comparisons between resident and migratory phenotypes within and between eastern and western clades. Overall, we find wide-spread support for parallel evolution at the genic level, particularly in genes that mediate biological timekeeping. However, we find little evidence of parallelism at the individual SNP level, supporting the idea that there are multiple genetic pathways involved in the modulation of migration.