We tested the hypothesis that increased telencephalon size has evolved in threespine stickleback fish (Gasterosteus aculeatus) from structurally complex habitats using field‐caught samples from one sea‐run (ancestral) and 18 ecologically diverse freshwater (descendant) populations. Freshwater habitats ranged from shallow, structurally complex lakes with benthic‐foraging stickleback (benthics), to deeper, structurally simple lakes in which stickleback depend more heavily on plankton for prey (generalists). Contrary to our expectations, benthics had smaller telencephala than generalists, but the shape of the telencephalon of the sea‐run and benthic populations were more convex laterally. Convex telencephalon shape may indicate enlargement of the dorsolateral region, which is homologous with the tetrapod hippocampus. Telencephalon morphology is also sexually dimorphic, with larger, less convex telencephala in males. Freshwater stickleback from structurally complex habitats have retained the ancestral telencephalon morphology, but populations that feed more in open habitats on plankton have evolved larger, laterally concave telencephala.