Rift Valley fever virus (RVFV) belongs to the order Bunyavirales and is the type species of genus Phlebovirus, which accounts for over 50% of family Phenuiviridae species. RNA-dependent RNA polymerase (L protein) is responsible for facilitating the replication and transcription of the virus. We report two cryo-EM RVFV L protein structures at 3.6 Å and 3.8 Å resolution in the presence and absence of RNA, respectively. In this first L protein structure of genus Phlebovirus, viral RNA induces considerable conformational changes of the polymerase. The RVFV L protein priming loop is distinctly different from those of other L proteins and undergoes large movements related to its replication elongation role. Structural and biochemical analyses indicate that a single template can initiate RNA replication, which is notably enhanced by 5’ viral RNA. These findings advance our understanding of RNA synthesis mechanism and provide a basis for antiviral inhibitor development.