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Radical environmental change that provokes population decline can impose constraints on the sources of genetic variation that may enable evolutionary rescue. Adaptive toxicant resistance has rapidly evolved in Gulf killifish ( Fundulus grandis ) that occupy polluted habitats. We show that resistance scales with pollution level and negatively correlates with inducibility of aryl hydrocarbon receptor (AHR) signaling. Loci with the strongest signatures of recent selection harbor genes regulating AHR signaling. Two of these loci introgressed recently (18 to 34 generations ago) from Atlantic killifish ( F. heteroclitus ). One introgressed locus contains a deletion in AHR that confers a large adaptive advantage [selection coefficient ( s ) = 0.8]. Given the limited migration of killifish, recent adaptive introgression was likely mediated by human-assisted transport. We suggest that interspecies connectivity may be an important source of adaptive variation during extreme environmental change.