Many organisms considered as strictly clonal may in fact experience some rare events of sexual reproduction with their sexual relatives. However, the rate of sexual–asexual gene flow has rarely been assessed mainly because its evaluation is difficult to achieve in the field. In the cyclically parthenogenetic aphid Rhopalosiphum padi, two main sets of lineages, differing in their investment in sexual reproduction and in their genetic attributes, co-exist even at a very fine scale: the ‘sexual’ lineages which have a full commitment to the sexual reproduction, and the ‘facultatively asexual’ lineages, which allocate investment in the sexual and parthenogenetic reproduction. This system offers a unique opportunity to tackle the genetic interactions between two contrasting reproductive modes. Here, we provide evidence that gene flow occurred between sexual and facultatively asexual lineages of R. padi. We carefully examined the shuffling in phenotypic and genotypic variation following a sexual reproduction event that took place in the field. Combining genotypic data and phenotypic measurements showed that this gene mixing led to the production of a wide array of reproductive modes, including strictly asexual lineages. Finally, we discuss the central role played by facultatively asexual lineages on the maintenance of reproductive mode variation.