Significance Unlike fellow nonsegmented negative-strand RNA viruses, exemplified by the devastating Nipah, Ebola, rabies, and measles viruses, vesicular stomatitis virus (VSV) can be considered beneficial, as it is widely used as a vector for anticancer therapy and vaccine development. In these RNA viruses, transcription and replication of the viral genome depend on an RNA-dependent RNA polymerase. Here, we determined the in situ structure of the VSV polymerase complex, consisting of a large protein (L) and a phosphoprotein (P), by cryo-electron tomography and subtomogram averaging. Approximately 55 polymerase complexes are packaged in each bullet-shaped virion through flexible interactions with nucleoproteins. Our results provide insights into the mechanism of L packaging during virus assembly and efficient initiation of transcription during infection.