Foraging behaviours encompass strategies to locate resources and to exploit them. In many taxa these behaviours are controlled by a major gene called for, but mechanisms vary between species. In the parasitoid wasp Venturia canescens, sexual and asexual populations coexist in sympatry but differ in their foraging behaviours. Here we explored the molecular bases underpinning this divergence in foraging behaviours by testing two mutually non-exclusive hypotheses: firstly the divergence in the for gene results in difference in foraging strategies, and second this latter is due to a divergence in whole-genome expression. Using comparative genomics, we showed that the for gene was conserved across insects considering both sequence as well as gene model complexity. Polymorphism analysis did not support the occurrence of two allelic variants diverging across the two populations, yet asexual population exhibited less polymorphism compared to the sexual one. Sexual and asexual transcriptomes sharply split up, with 10.9% of differentially expressed genes, but these were not enriched in behavioural related genes. We showed that the for gene was more expressed in asexual female heads than in sexual ones, and that asexuals were the ones that explored more the environment and exploited more host patches. Overall, these results suggested that a fine tuning in the for gene expression between populations may have led to distinct foraging behaviours. We hypothesized that reproductive polymorphism and coexistence in sympatry of sexual and asexual populations specialized to different ecological niches via divergent optima on phenotypic traits, could imply adaptation through different expression patterns of the for gene and at many other loci throughout the genome.