We investigated the diversity and transmission of RNA viruses during treatment of black soldier fly larvae (BSFL) with three typical organic wastes: waste-activated sludge (WAS), food waste (FW), and pig manure (PM). Metatranscriptomic analyses identified 175 RNA viral operational taxonomic units (vOTUs), 54.3% of which were novel, mainly affiliated with the Narna-Levi and Tombus-Noda supergroups. Viral communities in BSFL and frass were shaped by both insect-associated viruses (e.g., Inseviridae and Iflaviridae) and feedstock-derived viruses. While FW and wheat bran supported BSFL growth, the detected viruses were primarily associated with insects. PM and WAS introduced a broader range of plant-, fungus-, and vertebrate-infecting viruses, including zoonotic viruses such as Astroviridae and Picobirnaviridae. BSFL treatment eliminated Astrovirus from PM and markedly reduced human-pathogenic viruses (e.g., norovirus and enterovirus) within 6–8 days, while picobirnavirus persisted in frass. Frass also retained plant-infecting viruses (e.g., Virgaviridae) and novel Fiersviridae phages. Although BSFL treatment increased viral microdiversity (gene-level π ∼ 11-fold, nucleotide diversity of 7.33 × 10–5 to 8.31 × 10–4, decreased Tajima’s D), most pN/pS ratios remained <1, indicating that purifying selection predominated. These findings highlight organic wastes as reservoirs of diverse RNA viruses and the dynamic, feedstock-mediated, and BSFL-mediated shaping of viromes, emphasizing the need for integrated viral monitoring for safe resource recovery.
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