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Abstract Parasitoid wasps are one of the most species‐rich groups of animals on Earth, due to their ability to successfully develop as parasites of nearly all types of insects. Unlike most known parasitoid wasps that specialize towards one or a few host species,Diachasmimorpha longicaudatais a generalist that can survive within multiple genera of tephritid fruit fly hosts, including many globally important pest species.Diachasmimorpha longicaudatahas therefore been widely released to suppress pest populations as part of biological control efforts in tropical and subtropical agricultural ecosystems. In this study, we investigated the role of a mutualistic poxvirus in shaping the host range ofD. longicaudataacross three genera of agricultural pest species: two of which are permissive hosts forD. longicaudataparasitism and one that is a nonpermissive host. We found that permissive hostsCeratitis capitataandBactrocera dorsaliswere highly susceptible to manual virus injection, displaying rapid virus replication and abundant fly mortality. However, the nonpermissive hostZeugodacus cucurbitaelargely overcame virus infection, exhibiting substantially lower mortality and no virus replication. Investigation of transcriptional dynamics during virus infection demonstrated hindered viral gene expression and limited changes in fly gene expression within the nonpermissive host compared with the permissive species, indicating that the host range of the viral symbiont may influence the host range ofD. longicaudatawasps. These findings also reveal that viral symbiont activity may be a major contributor to the success ofD. longicaudataas a generalist parasitoid species and a globally successful biological control agent.