Despite their evident importance for function, dynamics of intrinsically unstructured proteins are poorly understood. Sendai virus phosphoprotein, cofactor of the RNA polymerase, contains a partly unstructured protein domain. The phosphoprotein X domain (PX) is responsible for binding the polymerase to the nucleocapsid assembling the viral RNA. For RNA synthesis, the interplay of the dynamics of the unstructured and structured PX subdomains is thought to drive progression of the RNA polymerase along the nucleocapsid. Here we present a detailed study of the dynamics of PX using hydrogen/deuterium exchange and different NMR relaxation measurements. In the unstructured subdomain, large amplitude fast motions were found to be fine-tuned by the presence of residues with short side chains. In the structured subdomain, where fast motions of both backbone and side chains are fairly restricted, the first helix undergoes slow conformational exchange corresponding to a local unfolding event. The other two helices, which represent the nucleocapsid binding site, were found to be more stable and to reorient with respect to each other, as probed by slow conformational exchange identified for residues on the third helix. The study illustrates the intrinsically differential dynamics of this partly unstructured protein and proposes the relation between these dynamics and its function.