In a previous study we described a Helitron transposon that apparently became one of the segments in the symbiotic Cotesia vestalis bracovirus (CvBV) from the parasitoid wasp C. vestalis. We presented evidence that this Helitron, named Hel_c35, invaded the C. vestalis genome through a horizontal transfer (HT) event from a dipteran and was later transferred horizontally from C. vestalis to a lepidopteran species. Based on the phylogeny of Hel_c35, we suggested that both HTs occurred in East Asia. We have also anticipated that, as more sequenced genomes from new species become available, more HTs involving Hel_c35 would be detected. Although the inclusion of Hel_c35 as a CvBV segment turned out to be a methodological artifact, the fact that Hel_c35 copies are present in the genomes of C. vestalis and other arthropods still remains. Here, we investigated the evolution of Hel_c35 in arthropods using an updated data set to reassess our previous findings. Most species (95%) included in the present work had their genomes sequenced after our initial study was published, thus representing new descriptions of taxa harboring Hel_c35. Our results expand considerably the number of putative HTs involving Hel_c35, with up to dozens of previously undescribed events, and suggest that the most recent HTs associated with C. vestalis took place in Europe. Considering the phylogenetic distribution of Hel_c35, and the evidence that its DNA sequences are present in the calyx fluid of C. vestalis and tissues from its parasitized host, we argue that many HT events were favored by the behavior of this wasp.