Japanese encephalitis virus (JEV), Usutu virus (USUV), and Murray valley encephalitis virus (MVEV) are emerging orthoflaviviruses of global significance. There are no approved therapeutics available and no vaccines for either MVEV or USUV. Given the close serological relationship of these viruses we aimed to structurally and antigenically characterise existing monoclonal antibodies (mAbs) to explore the potential for broadly neutralising mAbs against these viruses. Using a chimeric vaccine platform we functionally examined a panel of mAbs, identifying two human JEV mAbs, hJEV-9 and hJEV-7 with contrasting profiles. Binding and neutralisation against chimeric JEV (bJEV), USUV (bUSUV), and MVEV (bMVEV) showed that hJEV-7 was JEV specific while hJEV-9 bound and neutralised all three viruses, including the emerging JEV genotype 4 strain isolated from NSW in 2022. Both mAbs were then structurally characterised using cryo-electron microscopy (cryo-EM) single particle analysis (SPA), with structures of the fab fragments of hJEV-7 and hJEV-9 complexed with the vaccine strain of chimeric JEV (bJEV) resolved to 3.0 Å and 2.8 Å, respectively. This revealed hJEV-7 recognizes an epitope of the envelope (E) protein that spans the E domain I-II hinge region. By comparison, cryo-EM SPA of hJEV-9 bound to bJEV and bUSUV revealed a novel site and a previously unobserved virion occupancy for a flavivirus antibody. hJEV-9 binds only at the three-fold axis on the virion surface where it makes contacts with E domain III of one asymmetric unit and the E domain I-II hinge region of the neighbouring 3-fold E protein, forming a unique quaternary epitope spanning the mature virion raft formation. The broad neutralisation profile and conserved epitope of hJEV-9 across JEV, USUV and MVEV, makes it an ideal candidate for broad spectrum antibody therapy. Together, these structures present two novel JEV serocomplex epitopes and provide structural blueprints for future broad-spectrum vaccine and therapeutic design.