Abstract In a large behavioral experiment we reconstructed the evolution of behavioral responses to predators to explore how interactions with predators have shaped the evolution of their prey's behavior. All Enallagma damselfly species reduced both movement and feeding in the presence of coexisting predators. Some Enallagma species inhabit water bodies with both fish and dragonflies, and these species responded to the presence of both predators, whereas other Enallagma species inhabit water bodies that have only large dragonflies as predators, and these species only responded to the presence of dragonflies. Lineages that shifted to live with large dragonflies showed no evolution in behaviors expressed in the presence of dragonflies, but they evolved greater movement in the absence of predators and greater movement and feeding in the presence of fish. These results suggest that Enallagma species have evolutionarily lost the ability to recognize fish as a predator. Because species coexisting with only dragonfly predators have also evolved the ability to escape attacking dragonfly predators by swimming, the decreased predation risk associated with foraging appears to have shifted the balance of the foraging/predation risk trade-off to allow increased activity in the absence of mortality threats to evolve in these lineages. Our results suggest that evolution in response to changes in predation regime may have greater consequences for characters expressed in the absence of mortality threats because of how the balance between the conflicting demands of growth and predation risk are altered.