The genome of measles virus is encapsidated by multiple copies of the nucleoprotein (N), forming helical nucleocapsids of molecular mass approaching 150 Megadalton. The intrinsically disordered C-terminal domain of N (N _TAIL ) is essential for transcription and replication of the virus via interaction with the phosphoprotein P of the viral polymerase complex. The molecular recognition element (MoRE) of N _TAIL that binds P is situated 90 amino acids from the folded RNA-binding domain (N _CORE ) of N, raising questions about the functional role of this disordered chain. Here we report the first in situ structural characterization of N _TAIL in the context of the entire N-RNA capsid. Using nuclear magnetic resonance spectroscopy, small angle scattering, and electron microscopy, we demonstrate that N _TAIL is highly flexible in intact nucleocapsids and that the MoRE is in transient interaction with N _CORE . We present a model in which the first 50 disordered amino acids of N _TAIL are conformationally restricted as the chain escapes to the outside of the nucleocapsid via the interstitial space between successive N _CORE helical turns. The model provides a structural framework for understanding the role of N _TAIL in the initiation of viral transcription and replication, placing the flexible MoRE close to the viral RNA and, thus, positioning the polymerase complex in its functional environment.