The delineation of conservation units (CUs) is a challenging issue that has profound implications forminimizing the loss of biodiversity and ecosystem services. CU delineation typically seeks to prioritize evolutionary significance, and genetic methods play a pivotal role in the delineation process by quantifying overall differentiation between populations. Although CUs that primarily reflect overall genetic differentiation do protect adaptive differences between distant populations, they do not necessarily protect adaptive variation within highly connected populations. Advances in genomic methodology facilitate the characterization of adaptive genetic variation, but the potential utility of this information for CU delineation is unclear. We use genomic methods to investigate the evolutionary basis of premature migration in Pacific salmon, a complex behavioral and physiological phenotype that exists within highly connected populations and has experienced severe declines. Strikingly, we find that premature migration is associated with the same single locus across multiple populations in each of two different species. Patterns of variation at this locus suggest that the premature migration alleles arose from a single evolutionary event within each species and were subsequently spread to distant populations through straying and positive selection. Our results reveal that complex adaptive variation can depend on rare mutational events at a single locus, demonstrate that CUs reflecting overall genetic differentiation can fail to protect evolutionarily significant variation that has substantial ecological and societal benefits, and suggest that a supplemental framework for protecting specific adaptive variation will sometimes be necessary to prevent the loss of significant biodiversity and ecosystem services.