Anthropogenic habitat alterations can drive phenotypic changes in wild populations. However, the underlying mechanism (i.e., phenotypic plasticity and/or genetic evolution) and potential to recover previous phenotypic characteristics are unclear. Here we investigate the change in adult migration characteristics in wild salmon populations caused by dam construction and other anthropogenic habitat modifications. Strikingly, we find that dramatic allele frequency change from strong selection at a single locus explains the rapid phenotypic shift observed after recent dam construction.Furthermore, ancient DNA analysis confirms the abundance of a specific adaptive allele in historical habitat that will soon become accessible through a large restoration (i.e., dam removal) project.However, analysis of contemporary samples suggests the restoration will be challenged by loss of that adaptive allele from potential source populations. These results highlight the need to conserve and restore critical adaptive genetic variation before the potential for recovery is lost.