Our view of the biodiversity of animal viruses has been heavily biased toward humans and domestic and companion animals relevant to human livelihood, as was the arthropod vectors of human viruses. Here I will show how the meta-transcriptomic analysis of diverse animal taxa is helping to redefine the virosphere, provide critical new information on viral biodiversity, origins and evolution. Focusing on the orthomyxoviruses and flaviviruses I will how how the characterization of invertebrate species is helping to reveal the ancestry of many vertebrate viruses, challenging traditional classification systems, and highlighting that most RNA viruses are unlikely to be associated with disease in their hosts. On a broader scale, I will show how the analysis of invertebrates viruses has filled-in major phylogenetic “gaps” in the diversity of RNA viruses and has major implications for virus taxonomy, which may need a major revision, particularly given frequent lateral gene transfer and recombination among diverse viral species. Finally, there also appears to be a general reduction in the genome size of vertebrate compared to invertebrate RNA viruses, for reasons that are still unclear.