1.Plants exhibit impressive genetic and chemical diversity, not just between species but also within species, and the importance of plant intraspecific variation for structuring ecological communities is well known. When there is variation at the local population level, this can create a spatially‐heterogeneous habitat for specialized herbivores potentially leading to non‐random distribution of individuals across host‐plants. 2.Plant variation can affect herbivores directly and indirectly via a third species, resulting in variable herbivore growth rates across different host plants. Herbivores also exhibit within‐species variation, with some genotypes better adapted to some plant variants than others. 3.We genotyped aphids collected across two years from a field site containing ~200 patchily‐distributed host plants that exhibit high chemical diversity. The distribution of aphid genotypes, their ant mutualists, and other predators was assessed across the plants. 4.We present evidence that the local distribution of aphid (Metopeurum fuscoviride) genotypes across host‐plant individuals is associated with variation in the plant volatiles (chemotypes) and non‐volatile metabolites (metabotypes) of their host plant tansy (Tanacetum vulgare). Furthermore, these interactions in the field were influenced by plant‐host preferences of aphid‐mutualist ants. 5.Our results emphasize that plant intraspecific variation can structure ecological communities not only at the species level but also at the genetic level within species, and that this effect can be enhanced through indirect interactions with a third species.