There is considerable diversity in brain size within and among species, and substantial dispute over the causes, consequences and importance of this variation. Comparative and developmental studies are essential in addressing this controversy. Predation pressure has been proposed as a major force shaping brain, behaviour and life history. The Trinidadian guppy, Poecilia reticulata, shows dramatic variation in predation pressure across populations. We compared the brain mass of guppies from high and low predation populations collected in the wild. Male but not female guppies exposed to high predation possessed heavier brains for their body size compared to fish from low predation populations. The brain is a plastic organ, so it is possible that the population differences we observed were partly due to developmental responses rather than evolved differences. In a follow‐up study, we raised guppies under cues of predation risk or in a control condition. Male guppies exposed to predator cues early in life had heavier brains relative to their body size than control males, while females showed no significant effect of treatment. Collectively our results suggest that male guppies exposed to predation invest more in neural tissue, and that these differences are at least partly driven by plastic responses.