Intraguild predation is a common ecological interaction that occurs when a species preys upon another species with which it competes. The interaction is potentially a mechanism of divergence between intraguild prey populations, but it is unknown if cases of character shifts in intraguild prey are an environmental or evolutionary response. We investigated the genetic basis and inducibility of character shifts in threespine stickleback from lakes with and without prickly sculpin, a benthic intraguild predator. Wild populations of stickleback sympatric with sculpin repeatedly show greater defensive armor and water column height preference. We lab-raised stickleback from lakes with and without sculpin, as well as marine stickleback, and found that differences between populations in armor, body shape, and behavior persisted in a common garden. Within the common garden, we raised stickleback half-families from multiple populations in the presence and absence of sculpin. Although the presence of sculpin induced trait changes in the marine stickleback, we did not observe an induced response in the freshwater stickleback. Behavioral and morphological trait differences between freshwater populations thus have a genetic basis and suggest an evolutionary response to intraguild predation.