RNA viruses likely exist in every species of cellular life. However, our knowledge of the RNA virus biodiversity comes from those viruses that act as agents of disease in humans or economically important animals and plants, which only represent a tiny fraction of eukaryotic diversity. To explore a wider range of hosts, we examined the transcriptomes of diverse invertebrates, which contain ~220 species sampled across nine phyla, namely, Arthropoda, Annelida, Sipuncula, Mollusca, Nematoda, Platyhelminthes, Cnidaria, Echinodermata, and the Chordata Subphylum Tunicata. For many of the hosts, RNA viruses make-up a substantial proportion of total host RNA (i.e. >10% of all transcripts excluding host rRNA), suggesting their important role within the host RNA environment. The analyses also revealed 1445 previously undescribed divergent RNA virus species, many of which filled-in major gaps on the RNA virus phylogeny, and providing a more continuous landscape of genetic diversity between virus families and orders. Further analyses of the host distribution on the virus phylogenies revealed the presence of both host switching and long-term co-divergence in the deep evolutionary time-scale. The invertebrate RNA virome was also characterized by remarkable genomic flexibility, including frequent recombination, lateral gene transfer, and genomic re-arrangement, suggesting that a process of modular evolution has been commonplace. In summary, these data present a view of the virosphere that is more phylogenetically and genomically diverse than depicted in current classification schemes, and provides a new foundation for studies in RNA virus ecology and evolution.