Many species spend their lives in close association with other organisms, and the environments provided by those organisms can play an important role as causes of variation in phenotypes. When this is the case, the genotypes of the individuals constituting the environment may influence the phenotypes of individuals living in that environment. When these effects are between heterospecifics, interspecific indirect genetic effects (IIGEs) occur. Several studies have detected IIGEs, but whether IIGEs contribute to variation in sexually selected traits remains virtually unexplored. We assessed how mate preferences in a plant-feeding insect are influenced by the genotype of their host plant. We established clone lines of a sample of host plant genotypes constituting the background biotic environment for a random sample of insects that we reared on them. We found that the insects’ mate preferences varied according to the clone line on which they developed. These results demonstrate that genetic variation in host plants has cross-trophic consequences on a trait that has strong effects on fitness and interpopulation dynamics such as diversification in communication systems. We discuss how IIGEs on mate preferences may influence the way in which selection acts, including the maintenance of variation and the promotion of evolutionary divergence.