The African parasitoid wasp Cotesia sesamiae is structured in contrasted populations showing differences in host range and the recent discovery of a specialist related species, C. typhae, provide a good framework to study the mechanisms that link the parasitoid and their host range. To investigate the genomic bases of divergence between these populations, we used a targeted sequencing approach on 24 samples. We targeted a specific genomic region encoding the bracovirus, which is deeply involved in the interaction with the host. High sequencing coverage was obtained for all samples allowing the study of genetic variations between wasp populations and species. Combining population genetic estimations, the diversity (π), the relative differentiation (FST) and the absolute differentiation (dxy), and branch-site dN/dS measures, we identified six divergent genes impacted by positive selection belonging to different gene families. These genes are potentially involved in host adaptation and in the specialization process. Fine scale analyses of the genetic variations also revealed deleterious mutations and large deletions on certain genes inducing pseudogenization and loss of function. These results highlight the crucial role of the bracovirus in the molecular interactions between the wasp and its hosts and in the evolutionary processes of specialization.