Parasitoid wasps are insects that survive as obligate parasites that feed from and eventually kill their insect hosts. One of the most spectacular biological innovations that has repeatedly arisen in parasitoid wasp lineages is the evolution of heritable associations with viruses. Parasitoid wasps use these viruses as biological weapons that they introduce into host insects in order to subdue host defenses and alter host physiology to promote successful parasitism. Most known beneficial viruses share many features due to convergent evolution, which implies that these characteristics are important for the formation and persistence of parasitoid-virus associations. However, there is currently a major gap in knowledge pertaining to parasitoid viruses of diverse viral ancestry. Here, I conducted four studies to functionally and genetically characterize a novel virus inherited by Diachasmimorpha longicaudata wasps, known as Diachasmimorpha longicaudata entomopoxvirus (DlEPV). I first determined the replication and transmission dynamics of DlEPV within D. longicaudata wasps and their fruit fly hosts, then investigated the effects of the virus on wasp and fly health. My results indicated that DlEPV shares many features with other parasitoid viruses due to convergent evolution, but is also unique in aspects that are likely due to its poxvirus ancestry. Second, I sequenced the DlEPV genome and analyzed differences in viral activity between wasps and fly hosts. I found that, contrary to all other known beneficial viruses, DlEPV maintains a largely autonomous viral genome, and must use novel means to perpetuate its relationship with D. longicaudata. Third, I explored additional means of DlEPV transmission among wasps given the unique status of its genome. I determined that DlEPV utilizes post-hatch transmission that allows for highly efficient spread of the virus and its beneficial phenotype to wasps. Lastly, I investigated the possible effects of DlEPV on the host range of D. longicaudata by measuring DlEPV activity in fly species with varying permissiveness to D. longicaudata parasitism. I showed that DlEPV replication and virulence capabilities within fly hosts were strongly correlated with D. longicaudata parasitism ability, suggesting that DlEPV plays a major role in the success of D. longicaudata as a generalist parasitoid species.