Nipah Virus (NiV) is a highly-pathogenic emerging henipavirus with outbreaks on the Indian subcontinent and Malaysian peninsula regions. It has a high fatality rate causing death due to severe encephalitis or respiratory associated symptomology, and with no approved vaccines or therapeutics, requires increased research focus. Investigations into the molecular mechanism of viral-host membrane fusion of NiV have been previously undertaken, specifically focusing on the coordination between the receptor binding NiV Glycoprotein (NiVG) and the fusogen NiV Fusion (NiVF) proteins. Two proposed mechanisms describe the interaction; the clamp model stipulates NiVG stabilises the pre-fusion NiVF and the provocateur model stipulates NiVG activates the pre-fusion NiVF. We have used cryo-electron tomography and fluorescence energy resonance transfer to investigate the interactions of NiVF and NiVG before and after receptor binding, and particularly their distributions on the viral membranes. This has revealed a NiVF oligomerisation network that occurs on the surface of both NiV pseudovirions and virus-like particles, which partially occludes the fusion peptide, suggesting a self-stabilisation mechanism. Furthermore, we also present highly-potent neutralising single domain antibodies (sbAb) that bind to a quaternary crypt region of the NiVF protein. sdAbs were obtained through NiVF immunisation of a llama, generation of a library from peripheral blood mononuclear cells and enrichment via two rounds of phage display. They were characterised using bio-layer interferometry and cryo-electron microscopy single particle analysis revealing low nanomolar affinity to the NiVF pre-fusion ectodomain, and binding to a quaternary crypt. Pseudovirus neutralisation studies revealed neutralisation at low nanomolar IC50 values.