Tick-borne orthoflaviviruses (TBF), including tick-borne encephalitis virus (TBEV) and Powassan virus (POWV), remain a global concern with high case fatality rates, long-term disabling sequela, and continued emergence. Structural analysis of TBFs by cryogenic electron microscopy (cryo-EM) single particle analysis, a critical method to understanding virion structure and antibody interactions, requires large quantities of infectious virus and appropriate biocontainment levels – difficult for BSL3-4 TBFs. We sought to investigate a new system to safely produce authentic TBFs virions through an insect-specific flavivirus (ISF) chimeric platform. Chimeric orthoflaviviruses were produced by exchanging the pre-membrane and envelope proteins of Binjari virus (an ISF) with the corresponding genes of the pathogenic flavivirus. They are unable to replicate in vertebrate cells, including human neuronal cell line. Over ten TBF chimeras, including mammalian (TBEV, POWV, Omsk haemorrhagic fever, Alkhurma, Kyasanur Forest disease, Langat (LGTV), Gadgets Gully (GGYV)) and seabird viruses (Saumarez Reef; SREV) were constructed. Chimeric TBEV, POWV and LGTV were imaged by cryo-EM with high-resolution structures resolved by single particle analysis and asymmetric reconstruction and revealed structurally authentic virions. Multiple tick-borne orthoflavivirus neutralising monoclonal antibodies were recombinantly produced and used to validate these antigens in ELISA and neutralisation assays. The antigens were immunogenic in mice and neutralised wild-type viruses. We demonstrate a safe and efficient platform to study structure and antibody interactions of TBFs in BSL2 conditions. Additionally, we have shown that this platform produces promising antigens for TBF vaccine applications.