As a result of an intense host-parasite evolutionary arms race, parasitic wasps frequently display high levels of specialization on very few host species. For instance, in braconid wasps very few generalist species have been described. However, within this family, Cotesia sesamiae is a generalist species that is widespread in sub-Saharan Africa and develops on several lepidopteran hosts. In this study, we tested the hypothesis that C. sesamiae may be a cryptic specialist when examined at the intraspecific level. We sequenced exon 2 of CrV1, a gene of the symbiotic polyDNAvirus that is integrated into the wasp genome and is associated with host immune suppression. We found that CrV1 genotype was more closely associated with the host in which the parasitoid developed than any abiotic environmental factor tested. We also tested a correlation between CrV1 genotype and an infection with Wolbachia bacteria, which are known for their ability to induce reproductive isolation. The Wolbachia bacteria infection polymorphism was also found as a major factor explaining the genetic structure of CrV1, and, in addition, the best model explaining CrV1 genetic structure involved an interaction between Wolbachia infection and host species. We suggest that Wolbachia could act as an agent capable of maintaining advantageous alleles for host specialization in different populations of C. sesamiae. This mechanism could be applicable to other insect models because of the high prevalence of Wolbachia in insects.