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ABSTRACT For insects known as parasitoid wasps, successful development as a parasite results in the death of the host insect. As a result of this lethal interaction, wasps and their hosts have coevolved strategies to gain an advantage in this evolutionary arms race. Although normally considered to be strict pathogens, some viruses have established persistent infections within parasitoid wasp lineages and are beneficial to wasps during parasitism. Heritable associations between viruses and parasitoid wasps have evolved independently multiple times, but most of these systems remain largely understudied with respect to viral origin, transmission and replication strategies of the virus, and interactions between the virus and host insects. Here, we report a detailed characterization of Diachasmimorpha longicaudata entomopoxvirus (DlEPV), a poxvirus found within the venom gland of Diachasmimorpha longicaudata wasps. Our results show that DlEPV exhibits similar but distinct transmission and replication dynamics compared to those of other parasitoid viral elements, including vertical transmission of the virus within wasps, as well as virus replication in both female wasps and fruit fly hosts. Functional assays demonstrate that DlEPV is highly virulent within fly hosts, and wasps without DlEPV have severely reduced parasitism success compared to those with a typical viral load. Taken together, the data presented in this study illustrate a novel case of beneficial virus evolution, in which a virus of unique origin has undergone convergent evolution with other viral elements associated with parasitoid wasps to provide an analogous function throughout parasitism. IMPORTANCE Viruses are generally considered to be disease-causing agents, but several instances of beneficial viral elements have been identified in insects called parasitoid wasps. These virus-derived entities are passed on through wasp generations and enhance the success of the wasps’ parasitic life cycle. Many parasitoid-virus partnerships studied to date exhibit common features among independent cases of this phenomenon, including a mother-to-offspring route of virus transmission, a restricted time and location for virus replication, and a positive effect of virus activity on wasp survival. Our characterization of Diachasmimorpha longicaudata entomopoxvirus (DlEPV), a poxvirus found in Diachasmimorpha longicaudata parasitoid wasps, represents a novel example of beneficial virus evolution. Here, we show that DlEPV exhibits functional similarities to known parasitoid viral elements that support its comparable role during parasitism. Our results also demonstrate unique differences that suggest DlEPV is more autonomous than other long-term viral associations described in parasitoid wasps.