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ABSTRACT It is unclear how environmental change influences standing genetic variation in wild populations. Here, we characterised environmental conditions that protect versus erode polymorphic chemical defences inBoechera stricta(Brassicaceae), a short‐lived perennial wildflower. By manipulating drought and herbivory in a 4‐year field experiment, we measured the effects of driver variation on vital rates of genotypes varying in defence chemistry and then assessed interacting driver effects on total fitness (estimated as each genotype's lineage growth rate,λ) using demographic models. Drought and herbivory interacted to shape vital rates, but contrasting defence genotypes had equivalent total fitness in many environments. Defence polymorphism thus may persist under a range of conditions; however, ambient field conditions fall close to the boundary of putatively polymorphic environment space, and increasing aridity may drive populations to monomorphism. Consequently, elevated intensity and/or frequency of drought under climate change may erode genetic variation for defence chemistry inB. stricta.