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Dispersal of prey from predator-free patches frequently supplies a trophic subsidy to predators by providing more prey than are produced locally. Prey arriving from predator-free patches might also have evolved weaker defenses against predators and thus enhance trophic subsidies by providing easily captured prey. Using local models assuming a linear or accelerating trade-off between defense and population growth rate, we demonstrate that immigration of undefended prey increased predator abundances and decreased defended prey through eco-evolutionary apparent competition. In individual-based models with spatial structure, explicit genetics, and gene flow along an environmental gradient, prey became maladapted to predators at the predator's range edge, and greater gene flow enhanced this maladaptation. The predator gained a subsidy from these easily captured prey, which enhanced its abundance, facilitated its persistence in marginal habitats, extended its range extent, and enhanced range shifts during environmental changes, such as climate change. Once the predator expanded, prey adapted to it and the advantage disappeared, resulting in an elastic predator range margin driven by eco-evolutionary dynamics. Overall, the results indicate a need to consider gene flow-induced maladaptation and species interactions as mutual forces that frequently determine ecological and evolutionary dynamics and patterns in nature.