In moths, mate finding strongly rely on the detection of sex pheromones by pheromone receptors (PRs). Any modification in the functional properties of these receptors can have a drastic impact on reproduction. In the course of characterizing candidate PRs in the noctuid moth Spodoptera littoralis, we expressed them in Drosophila olfactory sensory neurons and stimulated them with a large panel of moth pheromone compounds. We found that two PRs detect (Z,E)-9,12-14:OAc, a minor component of the female pheromone blend. Whereas SlitOR6 is highly specific to this component, SlitOR13 is less sensitive and not strictly specific as it also detects (Z)9-14:OAc, another minor component of the sex pheromone. Interestingly, SlitOR13 expression is restricted to the distal part of male antennae, where we could identify a novel functional class of pheromone-sensitive neurons whose response spectrum matches that of SlitOR13. Based on a phylogenetic analysis of Lepidoptera PRs, we found that the ability to bind (Z,E)-9,12-14:OAc appeared independently within three paralogous lineages, and an analysis of selective pressures revealed sites under positive selection that could have played a role in the emergence of functional properties of OR6 and OR13 in Spodoptera species.