Most flaviviruses (family, Flaviviridae) are disease-causing pathogens of vertebrates maintained in zoonotic cycles between mosquitoes or ticks and vertebrate hosts. Poor sampling of flaviviruses outside vector-borne flaviviruses, such as Zika virus and dengue virus, have presented a narrow understanding of flavivirus diversity and evolution. In this study, we discovered three crustacean flaviviruses (Gammarus chevreuxi flavivirus, Gammarus pulex flavivirus and Crangon crangon flavivirus) and two cephalopod flaviviruses (Southern Pygmy squid flavivirus and Firefly squid flavivirus). Bayesian and Maximum-Likelihood phylogenetic methods demonstrate that crustacean flaviviruses form a well-supported clade and share a more closely related ancestor to terrestrial vector-borne flaviviruses than classical insect-specific flaviviruses. In addition, we identify variants of Wenzhou shark flavivirus in multiple gazami crab (Portunus trituberculatus) populations with active replication supported by evidence of an active RNA interference (RNAi) response. This suggests Wenzhou shark flavivirus moves horizontally between sharks and gazami crabs in ocean ecosystems. Analyses of the mono and dinucleotide composition of marine flaviviruses compared to flaviviruses with known host status suggest some marine flaviviruses share a nucleotide bias similar to vector-borne flaviviruses. Further, we identify crustacean flavivirus endogenous viral elements that are closely related to terrestrial vector-borne flaviviruses. Taken together, these data provide evidence of flaviviruses circulating between marine vertebrates and invertebrates, expand our understanding of flavivirus host range and offer potential insights into the evolution and emergence of terrestrial vector-borne flaviviruses.