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Abstract In a rapidly changing world, phenotypic plasticity may be a critical mechanism allowing populations to rapidly acclimate when faced with novel anthropogenic stressors. Theory predicts that if exposure to anthropogenic stress is heterogeneous, plasticity should be maintained as it allows organisms to avoid unnecessary expression of costly traits (i.e., phenotypic costs) when stressors are absent. Conversely, if exposure to stressors becomes constant, costs or limits of plasticity may lead to evolutionary trait canalization (i.e., genetic assimilation). While these concepts are well‐established in theory, few studies have examined whether these factors explain patterns of plasticity in natural populations facing anthropogenic stress. Using wild populations of wood frogs that vary in plasticity in tolerance to pesticides, the goal of this study was to evaluate the environmental conditions under which plasticity is expected to be advantageous or detrimental. We found that when pesticides were absent, more plastic populations exhibited lower pesticide tolerance and were more fit than less plastic populations, likely avoiding the cost of expressing high tolerance when it was not necessary. Contrary to our predictions, when pesticides were present, more plastic populations were as fit as less plastic populations, showing no signs of costs or limits of plasticity. Amidst unprecedented global change, understanding the factors shaping the evolution of plasticity will become increasingly important.