Study of the genetic and developmental architecture of mate preferences lags behind the study of sexual ornaments. This is in part because of the challenges involved in describing mate preferences, which are expressed as a function of variation in ornaments. We used the function-valued approach to test for genetic and environmental components of variation in female mate preferences in Enchenopa treehoppers (Hemiptera: Membracidae). These insects communicate with plant-borne vibrational signals, and offer a case study of speciation involving sexual selection and environmental change. We focused on female preferences for male signal frequency, the most divergent signal trait in Enchenopa. Obtaining complete, individual-level descriptions of mate preferences in a full-sib, split-family rearing experiment, we document substantial genetic variation in mate preference functions. Focusing on traits describing variation in the shape of the preference functions, we further document considerable broad-sense heritability and evidence of weak genotype × environment interaction in most traits. Against the background of recent and rapid divergence in Enchenopa, these results indicate potent mechanisms that maintain variation and sustain the involvement of mate preferences in sexual selection.