Significance Ebolaviruses belong to the group of nonsegmented negative strand (NNS) RNA viruses. Most members of the Ebolavirus genus cause severe disease in humans. Here, we report that ebolaviruses have evolved a genome replication mechanism that distinguishes them from the other NNS RNA viruses. The ebolavirus replication strategy includes the addition of a nontemplated 3′ nucleotide at the genome ends which may aid in avoiding antiviral recognition. Our data highlight the need for more research on NNS RNA virus replication strategies to reveal commonalities between virus families as well as unique features. Dissecting the replication mechanisms of NNS RNA viruses, including ebolaviruses, paves the way for the development of broad-spectrum antivirals that target the viral replication complexes, thereby preventing virus amplification.