Animal migration demands an interconnected suite of adaptations for individuals to navigate over long distances. This trait complex is crucial for small birds whose migratory behaviors—such as directionality—are more likely innate, rather than being learned as in many longer-lived birds. Identifying causal genes has been a central goal of migration ecology, and this endeavor has been furthered by genome-scale comparisons. However, even the most successful studies of migration genetics have achieved low resolution associations, identifying large chromosomal regions that encompass hundreds of genes, one or more of which might be causal. Here we leverage the genomic similarity among golden-winged (Vermivora chrysoptera) and blue-winged warblers (V. cyanoptera) to identify a single gene—Vacuolar Protein Sorting 13A (VPS13A)—that is associated with distinct differences in migration to Central American (CA) or South American (SA) wintering areas. We find reduced sequence variation in this gene-region for SA wintering birds, and show this is the likely result of natural selection on this locus. In humans, variants of VPS13A are linked to the neurodegenerative disorder chorea-acanthocytosis. This new association provides one of the strongest gene-level associations with avian migration differences.