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Abstract Phenotypic variation is common along environmental gradients, but it is often not known to what extent it results from genetic differentiation between populations or phenotypic plasticity. We studied populations of a livebearing fish that have colonized streams rich in toxic hydrogen sulphide (H2S). There is strong phenotypic differentiation between adjacent sulphidic and non-sulphidic populations. In this study, we varied food availability to pregnant mothers from different populations to induce maternal effects, a form of plasticity, and repeatedly measured life-history and behavioural traits throughout the ontogeny of the offspring. Genetic differentiation affected most of the traits we measured, in that sulphidic offspring tended to be born larger, mature later, have lower burst swimming performance, be more exploratory, and feed less effectively. In contrast, maternal effects impacted few traits and at a smaller magnitude, although offspring from poorly provisioned mothers tended to be born larger and be more exploratory. Population differences and maternal effects (when both were present) acted additively, and there was no evidence for population differences in plasticity. Overall, our study suggests that phenotypic divergence between these populations in nature is caused primarily by genetic differentiation and that plasticity mediated by maternal effects accentuates but does not cause differences between populations.