Polydnaviruses (PDVs) are fascinating viruses. Described in thousands of parasitoid wasp species they are unique viruses having both a segmented DNA genome in viral particles and an integrated form that persists as a provirus in the wasp genome. Parasitoid wasps inject their eggs in another insect host typically a lepidopteran. In these host-parasitoid interactions, the virus particles are co-injected along with the eggs and are essential to ensure wasp parasitism success. PDVs do not replicate in the lepidopteran host, but expression of viral gene products confers protection from the host immune defence response. Two genera of PDVs phylogenetically unrelated exist, the bracoviruses (BVs) and the ichnoviruses (IVs), associated with braconid and ichneumonid wasps, respectively. New data on the genomes of two bracoviruses (Microplitis demolitor BV and Cotesia congregata BV) and an ichnovirus associated with Campoletis sonorensis (CsIV) offers us new elements to discuss the central questions concerning the origin of these viral entities and how they have evolved. The results of sequencing approaches indicate that the tens of millions of years of mutualistic associations between PDVs and wasps have had a strong impact on PDV genomes that now ressemble eukaryotic regions both in organization and gene content.