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Atlantic killifish (Fundulus heteroclitus) residing in some urban and industrialized estuaries of theUSeastern seaboard demonstrate recently evolved and extreme tolerance to toxic aryl hydrocarbon pollutants, characterized as dioxin‐like compounds (DLCs). Here, we provide an unusually comprehensive accounting (69%) through quantitative trait locus (QTL) analysis of the genetic basis forDLCtolerance in killifish inhabiting an urban estuary contaminated withPCBcongeners, the most toxic of which areDLCs. Consistent with mechanistic knowledge ofDLCtoxicity in fish and other vertebrates, the aryl hydrocarbon receptor (ahr2) region accounts for 17% of trait variation; however,QTLon independent linkage groups and their interactions have even greater explanatory power (44%).QTLinterpreted within the context of recently availableFundulusgenomic resources and shared synteny among fish species suggest adaptation via interacting components of a complex stress response network. SomeQTLwere also enriched in other killifish populations characterized asDLC‐tolerant and residing in distant urban estuaries contaminated with unique mixtures of pollutants. Together, our results suggest thatDLCtolerance in killifish represents an emerging example of parallel contemporary evolution that has been driven by intense human‐mediated selection on natural populations.