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Abstract Behavioural plasticity is a major driver in the early stages of adaptation, but its effects in mediating evolution remain elusive because behavioural plasticity itself can evolve.In this study, we investigated how male Trinidadian guppies (Poecilia reticulata) adapted to different predation regimes diverged in behavioural plasticity of their mating tactic. We reared F2 juveniles of high‐ or low‐predation population origins with different combinations of social and predator cues and assayed their mating behaviour upon sexual maturity.High‐predation males learned their mating tactic from conspecific adults as juveniles, while low‐predation males did not. High‐predation males increased courtship when exposed to chemical predator cues during development; low‐predation males decreased courtship in response to immediate chemical predator cues, but only when they were not exposed to such cues during development.Behavioural changes induced by predator cues were associated with developmental plasticity in brain morphology, but changes acquired through social learning were not.We thus show that guppy populations diverged in their response to social and ecological cues during development, and correlational evidence suggests that different cues can shape the same behaviour via different neural mechanisms. Our study demonstrates that behavioural plasticity, both environmentally induced and socially learnt, evolves rapidly and shapes adaptation when organisms colonize ecologically divergent habitats.