Viruses significantly influence the functioning of marine ecosystem. However, our comprehension of viruses inhabiting the dark ocean remains limited. This is particularly so beneath Antarctic ice shelves, despite exerting a profound influence on global carbon cycle and climate system. Here, we uncover the viral diversity, biogeography, activity and their role as metabolic facilitators of microbes beneath the Ross Ice Shelf. The viral community was mainly comprised of novel, endemic viruses adapted to polar and mesopelagic environments. Extremely low abundance of genes related to lysogenic lifestyle (<3%) did not support a predominance of the Piggyback-the-Winner, consistent with a low productive habitat. Our results indicate a viral community actively infecting the key ammonium and sulfur-oxidizing chemolithoautotrophs (e.g. Nitrosopumilus spp, Thioglobus spp.), supporting a kill-the-winner. These viruses carry specific auxiliary metabolic genes involved in nitrogen, sulfur and phosphorus acquisition. Altogether, the viruses under Antarctic ice shelves are involved in reprograming the metabolism of ecologically cornerstone microbes that maintain primary production in these chemosynthetically-driven ecosystems, which have a major role in global nutrient cycles.