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The knowledge on symbiotic microorganisms of insects has increased in recent years, yet relatively little data is available on non-pathogenic viruses. Here we studied the virome of the parasitoid wasp Anagyrus vladimiri (Hymenoptera: Encyrtidae), a biocontrol agent of mealybugs. By high-throughput sequencing of viral nucleic acids, we revealed three novel viruses, belonging to the families Reoviridae (provisionally termed AnvRV [Anagyrus vladimiri reovirus]), Iflaviridae (AnvIFV) and Dicistroviridae (AnvDV). Phylogenetic analysis further classified the AnvRV in the genus Idnoreovirus, and the AnvDV in the genus Triatovirus. The genome of AnvRV is comprised of 10 distinct genomic segments ranging in length from 1.5 to 4.2 Kbp, but only two out of the 10 open reading frames (ORFs) have a known function. AnvIFV and AnvDV each have one polypeptide ORF, which is typical to iflaviruses but very un-common among dicistroviruses. AnvRV was found to be fixed in a mass-reared population of A. vladimiri, whereas it’s prevalence in field-collected wasps was ~15%. Similarly, the prevalence of AnvIFV and AnvDV were much higher in the mass rearing population than in the field population. Transmission electron micrographs of females’ ovaries revealed clusters and viroplasms of Reovirus-like particles in follicle cells. AnvRV was not detected in the mealybugs, suggesting that this virus is truly associated with the wasps. The possible effects of these viruses on A. vladimiri’s biology, and on biocontrol agents in general are discussed. Our findings identify RNA viruses as potential players involved in the multitrophic system of mealybugs, their parasitoids and other members of the holobiont.ImportanceDifferent biological control approaches use industrially mass-reared natural enemy insects to reduce damage of arthropod pests. Such mass-reared cultures may be positively and/or negatively affected by various microorganisms, including viruses. Yet, current knowledge on virus diversity, especially in arthropods, is limited. Here, we provide the first virome characterization of a member of the wasps family Encyrtidae - the member being the parasitoid Anagyrus vladimiri - a commercially important natural enemy of mealybug pests. We describe the genome of three previously unknown RNA viruses, co-inhabiting this parasitoid, and elaborate on the prevalence of those viruses in individual wasps of both mass-reared and environmental origins. Microscopy images suggest that at least one of the viruses is transmitted maternally via the ovaries. We discuss the genomic structure of the viruses and the possible relationship between those viruses and the A. vladimiri host, with implications on improvement of biocontrol of mealybug pests.