Intraguild predation – competition and predation by the same antagonist – is widespread, but its evolutionary consequences are unknown. Intraguild prey may evolve antipredator defenses, superior competitive ability on shared resources, or the ability to use an alternative resource, any of which may alter the structure of the food web. We tested for evolutionary responses by threespine stickleback to a benthic intraguild predator, prickly sculpin. We used a comparative morphometric analysis to show that stickleback sympatric with sculpin are more armored and have more limnetic-like body shapes than allopatric stickleback. To test the ecological implications of this shift we conducted a mesocosm experiment that varied sculpin presence and stickleback population of origin (from one sympatric and one allopatric lake). Predation by sculpin greatly increased the mortality of allopatric stickleback. In contrast, sculpin presence did not affect the mortality of sympatric stickleback, though they did have lower growth rates suggesting increased non-predatory effects of sculpin. Consistent with their morphology, sympatric stickleback included more pelagic prey in their diets, leading to depletion of zooplankton in the mesocosms. These findings suggest that intraguild prey evolution has altered food web structure by reducing both predation by the intraguild predator and diet overlap between species.