Summary 1. Plants express multiple defensive traits, but little is known about the genetic stability and phenotypic plasticity of these traits in nature. To investigate sources of variation and their potential ecological consequences for herbivores, we combined field observations of cyanogenic lima bean with laboratory experiments. 2. Field studies in South Mexico revealed a distinct variability of cyanogenic traits within and among wild lima bean populations. To differentiate among genetic variation and the impact of ambient conditions on plant phenotypes, we used seed-grown plants as well as clones propagated from high- (HC) and low-cyanogenic (LC) wild type plants. 3. In growth chamber experiments, we cultivated plants under three intensities each of drought and salt stress, nutrient supply, and light availability. We consecutively quantified cyanogenesis and total phenolics as chemical defences, soluble proteins as measure of leaf quality, and leaf mass per area and tissue hydration as physical defence-associated traits. 4. Plant traits were genetically stable, as clones propagated from the HC- and LC-mother plants maintained their cyanogenic features and also showed constancy of other leaf parameters tested. 5. In contrast to genetically heterogeneous seed-grown plants, cyanogenesis and soluble protein concentration in clonal plants showed significant variation in response to reduced water supply, increased soil salinity, and fertilization. The other leaf traits, however, showed no significant phenotypic plasticity depending on treatment. 6. Among all traits analysed, genetic and phenotypic variation in cyanogenesis proved the best predictor of herbivore behaviour and development, as LC-plants were preferred by adult Mexican bean beetles and allowed for faster larval development. 7.Synthesis. We demonstrate that (i) functional analyses of plant responses to abiotic factors require methodical separation of genotypic variability and phenotypic plasticity, (ii) different abiotic parameters quantitatively affect the plants’ chemical phenotype and that (iii) changes of plant phenotype can have strong impacts on natural herbivores. Our results suggest that genetic variability and phenotypic plasticity of plant anti-herbivore defences allow plant populations to rapidly respond to changing environmental conditions.