Herbivorous insects exhibit strong feeding preferences when choosing among plant genotypes, yet experiments to map loci mediating plant susceptibility to herbivory rarely incorporate host choice. To address this gap, we applied genome-wide association (GWA) mapping to uncover genetic polymorphisms mediating damage from foraging insects (two populations of Scaptomyza flava) across a mixture of Arabidopsis thaliana genotypes in experimental enclosures. The effect of chemical defenses (glucosinolates) on herbivory depended on herbivore genotype. Unlike many studies that minimize the effects of host choice behavior, we also found a large effect of plant size on herbivory-likely through its effect on plant apparency-that was independent of herbivore genotype. These herbivory-associated loci are polymorphic at fine spatial scales, and thus have potential to shape variation in herbivory within natural populations. We also show that the polymorphism with the largest effect on herbivory underlies adaptive latitudinal variation in Arabidopsis plant size across Europe. Overall, our results provide genetic support for ecological observations that variation in both chemical defenses and non-canonical defense traits (e.g., plant size and phenology) jointly shapes plant-herbivore interactions.Interactions between plants and herbivores drive fundamental ecological and evolutionary processes. Herbivores remove 5-20% of the leaf tissue produced annually by plants 1, 2 , which reduces plant fitness 3, 4 , selects against susceptible plant genotypes 4-6 , and in turn shapes the composition of ecological communities through effects that cascade across trophic levels 7 . Understanding the mechanistic bases of plant-herbivore interactions is therefore a major goal in biology and agriculture [8][9][10] .Within plant species, individuals incur different amounts of damage from herbivores, and genetic differences among individuals explain a substantial proportion of this variation (e.g., 11 ). Identifying and characterizing specific genetic polymorphisms that shape herbivoryrelated phenotypes within plant populations, which we refer to as a gene-focused approach, offers a number of advantages for understanding how this variation arises and why it persists [12][13][14][15] . First, in-depth functional studies of genes harboring these variants can uncover specific biochemical and physiological processes that mediate interactions with herbivores 4 . Second, phenotypic comparisons among natural plant accessions or genetically engineered genotypes that vary at genes of interest can reveal how susceptibility to herbivory is linked to or trades off with other traits, including those of interest to evolutionary biologists (e.g., plant reproductive success 16 ) or crop breeders (e.g., plant biomass or yield). Third, population genetic studies, in which patterns at genes of interest are compared with neutral polymorphisms across the genome, can reveal how environmental pressures shape adaptive genetic variation within and among populations at loci a...