From screening published transcriptome data, we have identified 83 different virus genomes and virus-like sequences within 28 species of parasitic nematodes. As these parasites infect >1.5 billion people and animals globally, this finding may have broad-ranging impacts for almost a quarter of humanity and economically important livestock. Our analysis shows extensive diversity and a conserved global spread of virus/nematode associations across multiple continents suggesting an ancestral acquisition event and host-virus co-evolution. Focussing on the viruses of the filarial parasites Brugia malayi (Togaviridae, related to Alphaviruses) and Onchocerca volvulus (Rhabdoviridae, related to Lyssaviruses) reveals an intimate relationship, with the viruses localising within the reproductive tracts of both species, and being detectable in all laboratory isolates (B. malayi) as well as multiple isolates across Sub-Saharan Africa (O. volvulus). Viruses of B. malayi were also found to localise within cuticular inflations, or ‘bosses’ that were previously described in the literature, but with no known purpose. Additionally, we were able to show that the final mammalian host of these filarial parasites elicit antibody responses against the viruses demonstrating exposure to host immunity. This observation, as well as the intimate, chronic and life-long exposure to vertebrate tissues that typically characterise parasitic nematode infections, raise questions as to the role this previously hidden virome plays in modulating anti-parasite immunity, and their potential for influencing paasite biology and disease pathogenesis.