The family Flaviviridae of RNA viruses contains several notorious human pathogens such as dengue virus, West Nile virus, and hepatitis C virus. To date, however, our understanding of the biodiversity and evolution of the Flaviviridae has largely been directed toward mammalian hosts and their blood-feeding arthropod vectors. To better understand their diversity, evolutionary history and genomic flexibility, we used RNA-seq to search for the viruses related to the Flaviviridae in a range of invertebrate and vertebrate hosts. Accordingly, we recovered the full genomes of 5 segmented Jingmenviruses and 12 distant relatives of the known Flaviviridae (‘flavi-like’ viruses) from a range of arthropod hosts. These viruses are highly divergent, but share a similar genomic plan and common ancestry with the Flaviviridae at NS3 and NS5 regions. Remarkably, while these viruses fill in major gaps in the phylogenetic diversity of the Flaviviridae, genomic comparisons reveal the occurrence of important changes during their evolutionary history, including different genome structures, genome sizes, number of segmentation, and replication/gene regulation strategies. In addition, the wide diversity of flavi-like viruses found in invertebrates, as well as their deep phylogenetic positions, suggests that they may represent the ancestral forms from which the vertebrate-infecting viruses evolved. For the vertebrate viruses, we expanded the previously mammal-only pegivirus-hepacivirus group to include a virus from the graceful catshark (Proscyllium habereri), which in turn implies that these viruses possess a larger host range than is currently known. In sum, our data show that the Flaviviridae infect a far wider range of hosts and exhibit greater flexibility in genome structure than previously anticipated.