Parasitoid wasps of the Ichneumonoidea superfamily have repeatedly endogenized and retained functional sets of viral genes within their genomes. These functional viral genes have been co-opted by the wasps to produce viral particles in the reproductive tracts of females that are then injected during parasitism to assist the development of wasp progeny in host insects. Interestingly, several instances of endogenization and domestication in ichneumonoid wasps have been reported for viruses of the Nudiviridae family. Given these repeated events of viral co-option, hypotheses concerning the cooperative mechanism(s) used for retention and control over viral replication by these wasps have been proposed. However, thorough investigations into these cooperative mechanisms are severely lacking. Here, I investigate the regulatory mechanisms of controlling virus replication in two ichneumonoid wasps, Microplitis demolitor and Venturia canescens, and their associated viruses M. demolitor Bracovirus (MdBV) and V. canescens Endogenous Nudivirus (VcENV), respectively. First, I applied single-cell RNA sequencing (scRNA-seq) and single-cell assay for transposase accessible chromatin sequencing (scATAC-seq) on adult M. demolitor ovaries to profile the transcriptomes and chromatin of virus-producing cells. scRNA sequencing allowed for the identification of several populations of virus-producing cells, and a further characterization of MdBV replication dynamics. scATAC-seq of adult M. demolitor ovaries found unexpected and non-canonical pattens of chromatin accessibility near MdBV genes. Six candidate wasp genes were identified with putative roles for controlling MdBV replication. Second, I utilized a similar framework in V. canescens by employing single-cell multiome sequencing (scMulti-seq) on adult ovaries. ScMulti-seq combines the power of scRNA-seq and scATAC-seq by profiling the chromatin and transcriptome of individual nuclei. scRNA-seq determined several populations of virus-producing cells present in adult ovaries, each undergoing different stages of VcENV replication. scATAC-seq also found non-canonical chromatin patterns near VcENV genes, however this accessibility was also shown to be specific to virus-producing cells. In summary, 15 candidate wasp genes were identified for putative regulatory roles in VcENV replication, with strong support for the transcription factor Sox2-like.