Abstract: Although asexual lineages evolved from sexual lineages in many different taxa, the genetics of sex loss remains poorly understood. We addressed this issue in the pea aphid Acyrthosiphon pisum, whose natural populations encompass lineages performing cyclical parthenogenesis (CP) and producing one sexual generation per year, as well as obligate parthenogenetic (OP) lineages that can no longer produce sexual females but can still produce males. An SNP-based, whole-genome scan of CP and OP populations sequenced in pools (103 individuals from 6 populations) revealed that an X-linked region is associated with the variation in reproductive mode. This 840-kb region is highly divergent between CP and OP populations (F ST = 34.9%), with >2,000 SNPs or short Indels showing a high degree of association with the phenotypic trait. In OP populations specifically, this region also shows reduced diversity and Tajima's D, consistent with the OP phenotype being a derived trait in aphids. Interestingly, the low genetic differentiation between CP and OP populations at the rest of the genome (F ST = 2.5%) suggests gene flow between them. Males from OP lineages thus likely transmit their op allele to new genomic backgrounds. These genetic exchanges, combined with the selection of the OP and CP reproductive modes under different climates, probably contribute to the long-term persistence of the cp and op alleles. Significance: Asexual taxa occur in all major clades of eukaryotes and derive from sexual species. Yet, the genetic basis of these transitions is poorly understood because crosses cannot generally be performed to genetically map the ability to propagate asexually. As a result, a gene presumably responsible for sex loss has been identified in only one animal species—the Cape honeybee. Here, using pooled genome sequencing, we identified a 840-kb region (carrying 32 genes) that is associated with the transition to permanent asexuality in the pea aphid. We also revealed that sexual and asexual alleles likely diverged several hundred thousand years ago and that asexual lineages probably persist through contagious asexuality, whereby the few males they produce transmit asexual genes to sexual lineages. These results provide new insights into the mechanisms of coexistence of sexual and asexual lineages.