Horizontal gene transfer (HGT)—the movement of genetic material between species—has been reported across all major eukaryotic lineages. However, the underlying mechanisms of transfer and their impact on genome evolution are still poorly understood. While studying the evolutionary origin of a selfish element in the nematode C. briggsae, we discovered that Mavericks, ancient virus-like transposons related to giant viruses and virophages, are one of the long-sought vectors of horizontal gene transfer. Mavericks—also known as Polintons—are found in almost every major eukaryotic lineage. They are flanked by terminal inverted repeats and can readily jump and insert into genomes, like transposons. But like viruses, they code for a large number of proteins, including a type-B DNA polymerase, a retroviral-like integrase, as well as major and minor capsid proteins. Using a combination of phylogenetics, structural predictions and genetic crosses, we discovered that two novel nematode gene families—wosp proteases and krma kinases—are preferentially taken up as cargo genes by Mavericks and have been extensively transferred between different nematode species on a global scale. We also found that nematode Mavericks captured a novel fusogen, MFUS-1, which is structurally similar to the glycoprotein B from Herpes simplex virus 1. This event likely fueled their spread via the formation of enveloped infective particles, analogous to the inception of retroviruses from genomic retroelements. Lastly, we show how the union between a horizontally transferred wosp protease, msft-1, and a MULE transposon gave birth to a novel class of selfish gene in C. briggsae: a mobile toxin-antidote element that causes genetic incompatibilities that drive in wild populations. Our results identify the first wide-spread vector of HGT in animals and highlight how the intertwined biology of viruses and transposons can ultimately impact gene flow between populations, shaping the evolution of the species that carry them.