Whole genome duplication provides evolutionary opportunities to increase biological complexity and phenotypic diversity by selective retention of duplicated genes. We identify a small genomic region associated with complex phenotypic variation on duplicate copies of the same ancestral chromosome in salmon (Salmonidae). Across six species, three large-effect loci involved in migration timing, reproduction, and maturation are located in this genomic region. Life history and whole genome resequencing data support lineage-specific evolution of polymorphism related to early- and late-migrating phenotypes. The high frequency of transcription factors and lack of non-synonymous mutations suggests this region influences gene expression rather than modifying gene function. Repeated evolution of large-effect loci in multiple salmon species provides evidence of adaptive evolution facilitated by the salmonid specific whole genome duplication.