Intricate coevolutionary relationships between certain insect and plant lineages act as a possible explanation for the vast biodiversity of their species. The evolutionary ‘arms race’ of coevolution often drives many insect taxa to diversify, specialize, and even speciate more frequently than other animals. Because seed beetles impose a particularly intense selective pressure on their host plants (by directly consuming plant offspring), they have undergone widespread specialization to these plants. Thus, it is highly unusual to come across seed beetles that are considered relative generalists. The Great Plains seed beetle, Acanthoscelides fraterculus, presents a mystery as it has been reared from host plants across diverse genera. To determine whether A. fraterculus is a true generalist or is instead composed of many specialist populations (or even species), I conducted a natural experiment across geographically disparate sites with co-occurring host plants to untangle the geographic and coevolutionary influences that drive diversification. I analyzed the genotypic variation of A. fraterculus populations across Colorado and identified three distinctly host-associated specialized populations within this one previously defined species. I find that A. fraterculus appears to be in the midst of diversifying, and subpopulations feeding on non-ancestral host-plant genera reveal population structures in support of coevolution.