Horizontal transfer (HT) of DNA is an important factor shaping eukaryote evolution. Although several hundreds of eukaryote-to-eukaryote HTs of transposable elements (TEs) have been reported, the vectors underlying these transfers remain elusive. Here, we show that multiple copies of two TEs from the cabbage looper (Trichoplusia ni) transposed in vivo into genomes of the baculovirus Autographa californica multiple nucleopolyhedrovirus (AcMNPV) during caterpillar infection. We further demonstrate that both TEs underwent recent HT between several sympatric moth species (T. ni, Manduca sexta, Helicoverpa spp.) showing different degrees of susceptibility to AcMNPV. Based on two independent population genomics data sets (reaching a total coverage >330,000X), we report a frequency of one moth TE in ~8,500 AcMNPV genomes. Together, our results provide strong support for the role of viruses as vectors of TE HT between animals, and they call for a systematic evaluation of the frequency and impact of virus-mediated HT on the evolution of host genomes.