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Summary The chemical arms race between plants and insects is foundational to the generation and maintenance of biological diversity. We asked how the evolution of a novel defensive compound in an already well‐defended plant lineage impacts interactions with diverse herbivores.Erysimum cheiranthoides(Brassicaceae), which produces both ancestral glucosinolates and novel cardiac glycosides, served as a model.We analyzed gene expression to identify cardiac glycoside biosynthetic enzymes inE. cheiranthoidesand characterized these enzymes via heterologous expression and CRISPR/Cas9 knockout. UsingE. cheiranthoidescardiac glycoside‐deficient lines, we conducted insect experiments in both the laboratory and field.EcCYP87A126 initiates cardiac glycoside biosynthesis via sterol side‐chain cleavage, andEcCYP716A418 has a role in cardiac glycoside hydroxylation. In EcCYP87A126knockout lines, cardiac glycoside production was eliminated. Laboratory experiments with these lines revealed that cardiac glycosides were highly effective defenses against two species of glucosinolate‐tolerant specialist herbivores, but did not protect against all crucifer‐feeding specialist herbivores in the field. Cardiac glycosides had lesser to no effect on two broad generalist herbivores.These results begin elucidation of theE. cheiranthoidescardiac glycoside biosynthetic pathway and demonstratein vivothat cardiac glycoside production allowsErysimumto escape from some, but not all, specialist herbivores.