Borna disease virus (BDV) causes an infection of the central nervous system in a wide range of vertebrates, which can fatally progress to an immune-mediated disease, called Borna disease. BDV is a member of the Mononegavirales, which also includes the highly infectious measles and Ebola viruses. The viral nucleoproteins are central to transcription, replication, and packaging of the RNA genome. We present the X-ray structure of the BDV nucleoprotein determined at 1.76 A resolution. The structure reveals a novel fold, organized into two distinct domains, and an assembly into a planar homotetramer. Surface potential calculations strongly support an RNA binding model with the RNA wrapping around the outside of the tetramer, although a positively charged central channel in the tetramer could fit single-stranded RNA in an alternative binding mode. This first structure of an RNA virus nucleoprotein provides a paradigmatic model for RNA packaging and replication of single-stranded RNA viruses.