The great diversity of specialist plant-feeding insects suggests that host plant shifts may initiate speciation, even without geographic barriers. Pheromones and kairomones mediate sexual communication and host choice, and the response to these behaviour-modifying chemicals is under sexual and natural selection, respectively. The concept that the interaction of mate signals and habitat cues facilitates reproductive isolation and ecological speciation is well established, while the traits and the underlying sensory mechanisms remain unknown. The larva of codling moth feeds in apple and other rosaceous fruits. We show for the first time that the response of male moths to female sex pheromone codlemone relies upon presence of pear ester, a kairomone emitted by host fruit. In the non-host tree birch, attraction to pheromone alone is very strongly reduced, but is fully rescued by blending pheromone with kairomone. This affords a mechanism how host plant shifts shape new mate-finding signals that can give rise to assortative mating and reproductive isolation.