Over the last decade our group have discovered several insect-specific flaviviruses (ISFs) in mosquitoes from different regions of Australia. These viruses do not replicate in vertebrate cells but grow to high titre in mosquito cultures. Genome sequence analyses of these viruses reveal we have discovered many new species of ISFs representing two distinct genetic lineages. Construction of infectious DNAs and chimeric viruses has allowed us to identify stages at pre- and post-cell entry where ISF infection and replication is blocked in vertebrate cells. We have also generated a series of chimeric viruses expressing the structural genes (prM-E) from pathogenic flaviviruses, including West Nile, Zika and dengue viruses, spliced into the genetic backbone of two different ISF species. These chimeras exhibit the insect-specific phenotype of their parental ISFs, growing efficiently in mosquito cells but not in vertebrate cultures but are structurally indistinguishable from virions of the pathogenic parental viruses. These chimeric viruses are proving to be excellent candidates for safe diagnostic antigens and vaccines for mosquito-borne flaviviral diseases.