Henipaviral entry and infection occurs by direct virus-host cell membrane fusion by a similar mechanism, the formation of pathological syncytia occurs by cell-cell membrane fusion. Both viral-cell and cell-cell membrane fusion are coordinated by the receptor-binding attachment (G) and fusion (F) glycoproteins. Typically, the attachment protein binds the cognate host-cell receptor (ephrinB2 or ephrinB3) and undergoes a series of conformational changes that ultimately leads to exposure of the stalk domain that in turn triggers the fusion protein. In due course, the fusion protein proceeds to undergo a series of conformational changes as it progresses through the fusion cascade. Using henipaviruses as a model for the broader Paramyxovirus family, we identified novel domains between the henipaviral G and F proteins that affect fusion. Further, we identified conserved henipaviral regions within the fusion glycoprotein that affect distinct steps of the fusion cascade. First, we examine the fusion capacities between homologous and heterologous pairs of Nipah (NiV) and Hendra (HeV) G and F proteins and found that the heterologous pair of NiV-G and HeV-F is hyperfusogenic. We further determine the overall domains in G and F that contribute to affects in fusion through construction of NiV and HeV G and F chimeras. Secondly, we examine the roles of several F regions: the HR3, N1 and N4 in membrane fusion. These regions are initially in close proximity to the fusion peptide and/or undergo secondary structural changes between the pre-fusion and post-fusion F conformations. Here, by performing alanine scan mutagenesis and various functional analyses, we report that specific residues within these domains modulate the fusogenic capacity of NiV-F. Importantly, we defined the steps in the fusion cascade that these mutants affect. The roles of these domains and regions in the membrane fusion cascade have never been described before and may be common amongst other paramyxoviruses, thus providing promising targets for drug design. Moreover, our studies provide a new important understanding of how certain domains between G and F and certain regions within F modulate fusion.