Rapid glacier retreat is dramatically altering ecosystem dynamics and increasing meltwater outflow into populated areas, with significant implications for microbial and viral contributions to downstream systems. Understanding microbial-virome interactions is essential to predict what will be released from these melting glaciers. Using a metagenomic and metatranscriptomic approach, this study reveals that the Rhone glacier microbiome is dominated by bacteria and microeukaryotes, while the associated metavirome comprises viruses infecting both groups. Caudoviricetes predominantly target bacteria, while certain eukaryotic viruses, such as those in the Megaviricetes class, exhibit prokaryotic signatures, pointing to complex viral-host interactions. Viral host specificity ranges from highly targeted to broad-spectrum infectivity. Genomic analyses uncovered variable regions, including metagenomic and metaviromic islands enriched with genes involved in replication, recombination, repair, and transposable elements. Auxiliary metabolic genes were identified, primarily modifying bacterial methylation patterns to evade host defenses. These findings highlight the pivotal role of viruses in shaping microbial dynamics within glacier ecosystems and their potential environmental impact as glaciers continue to retreat.