Predator-prey interactions often vary markedly across natural landscapes. One explanation for this variation is local genetic differentiation of prey traits due to selection from predators. Here, I evaluated the relative contributions of selection from a gape-limited predator (Ambystoma opacum) and spatial location within a larger landscape to explanations of variation in foraging, growth, and survival in 10 populations of temporary pond breeding salamander larvae (Ambystoma maculatum). In parameterized models, high gape-limited predation risk was predicted to select for intense foraging and rapid growth in larvae when migration rates were low (less than 5%). Under common garden conditions, salamander larvae from populations naturally exposed to constant predation risk from A. opacum foraged more actively than those from populations faced with lower predation risks. Higher foraging rates were associated with lower survival in populations exposed to free-ranging A. opacum predators. These results demonstrate for the first time that prey hunger can evolve in a natural landscape of variable gape-limited predation risk depending on natural selection for growth into a size refuge. Moreover, evidence suggests that foraging-predation risk tradeoffs can evolve over microgeographic scales. However, foraging rates also appear to have been affected by gene flow: prey individuals from populations with high predation risk foraged more actively if located within regions with similar predation threats. This interaction between local selection and spatial location suggests a joint role for adaptation and maladaptation in shaping species interactions across natural landscapes, a finding with implications for dynamics at the population, community, and metacommunity levels.