The genus Henipavirus (HNV) includes highly pathogenic zoonotic viruses originating from bats, such as Nipah virus (NiV) and Hendra virus (HeV), for which no vaccines exist for humans. Moreover, a recent outbreak caused by novel shrew-borne HNV like Langya virus (LayV) in humans has highlighted the spillover potential of these viruses. Recently, two shrew-borne HNVs, Daeryong (DarV) and Gamak virus (GmkV), along with a bat-borne HNV, Angavokely virus (AngV), have been described. Notably, GakV has been found capable of infecting mammalian cell lines, but the potential for these viruses to cause disease in humans is uncertain due to limited characterisation. HNVs enter host cells by membrane fusion, mediated by receptor binding protein (RBP) and fusion (F) glycoproteins, which are also the main targets of humoral immunity. Here, we present the prefusion F protein structure of HNVs determined by cryogenic transmission electron microscopy. Despite sharing only approximately 40% sequence identity with prototypical HNV like NiV and HeV, they adopt a largely similar overall architecture. Furthermore, well-characterised anti-NiV and HeV neutralising F antibodies do not react to AngV, DarV or GakV F proteins. These findings suggest that newly described bat and shrew-borne HNV are antigenically divergent from the prototypical HNVs. By determining the structure of divergent HNV F proteins, this work provides a foundation for the development of new vaccines and therapeutics and enables pandemic preparedness against potential outbreaks of novel HNVs in the future.