To understand the dynamic interactions between the phosphoprotein (P) and the nucleoprotein (N) within the transcription/replication complex of the $Paramyxoviridae$ and to decipher their roles in regulating viral multiplication, we characterized the structural properties of the C-terminal X domain (P$_{XD}$) of Nipah (NiV) and Hendra virus (HeV) P protein. In crystals, isolated NiV P$_{XD}$ adopted a two-helix dimeric conformation, which was incompetent for binding its partners, but in complex with the C-terminal intrinsically disordered tail of the N protein (NTAIL), it folded into a canonical 3H bundle conformation. In solution, SEC-MALLS, SAXS and NMR spectroscopy experiments indicated that both NiV and HeV P$_{XD}$ were larger in size than expected for compact proteins of the same molecular mass and were in conformational exchange between a compact three-helix (3H) bundle and partially unfolded conformations, where helix $\alpha_3$ is detached from the other two. Some measurements also provided strong evidence for dimerization of NiV P$_{XD}$ in solution but not for HeV P$_{XD}$. Ensemble modeling of experimental SAXS data and statistical-dynamical modeling reconciled all these data, yielding a model where NiV and HeV P$_{XD}$ exchanged between different conformations, and where NiV but not HeV P$_{XD}$ formed dimers. Finally, recombinant NiV comprising a chimeric P carrying HeV P$_{XD}$ was rescued and compared with parental NiV. Experiments carried out in cellula demonstrated that the replacement of P$_{XD}$ did not significantly affect the replication dynamics while caused a slight virus attenuation, suggesting a possible role of the dimerization of NiV P$_{XD}$ in viral replication.