A 2.7 Å cryo-EM structure of the human parainfluenza virus type 3 (hPIV3) L–P complex with a second L protein's connector domain (CD') is reported, revealing the structural basis of dimerization and the active site of the polymerase. The study shows that the hPIV3 L protein adopts a unique β-strand latch, essential for polymerase activity. The L–L dimerization is crucial for RNA replication, as disruption of the L–L interface leads to replication defects that can be overcome by complementation. The structure highlights the conserved motifs and residues involved in polymerase function, and provides insights into the structural conservation and conformational changes of the polymerase. The study also reveals the structural basis of L–L dimerization, with CD' located at the putative template entry of the adjoining L. The findings suggest a new avenue for rational drug design against nsNSVs. The study provides a detailed understanding of the nsNSV polymerase structure and function, and the structural basis of L–L dimerization. The results demonstrate that the dimeric hPIV3 L–P complex is necessary for RNA replication, and that the L–P complex plays a role in RNA replication and encapsidation. The study also highlights the importance of the L–P interaction in the polymerase function and provides a structural model for RNA replication in nsNSVs. The findings contribute to the understanding of the structure-function properties of nsNSV polymerases and provide a more complete picture of the different conformations that the polymerase can adopt. The study also provides a potential novel avenue for antiviral drug design by targeting the polymerase dimer interface.A 2.7 Å cryo-EM structure of the human parainfluenza virus type 3 (hPIV3) L–P complex with a second L protein's connector domain (CD') is reported, revealing the structural basis of dimerization and the active site of the polymerase. The study shows that the hPIV3 L protein adopts a unique β-strand latch, essential for polymerase activity. The L–L dimerization is crucial for RNA replication, as disruption of the L–L interface leads to replication defects that can be overcome by complementation. The structure highlights the conserved motifs and residues involved in polymerase function, and provides insights into the structural conservation and conformational changes of the polymerase. The study also reveals the structural basis of L–L dimerization, with CD' located at the putative template entry of the adjoining L. The findings suggest a new avenue for rational drug design against nsNSVs. The study provides a detailed understanding of the nsNSV polymerase structure and function, and the structural basis of L–L dimerization. The results demonstrate that the dimeric hPIV3 L–P complex is necessary for RNA replication, and that the L–P complex plays a role in RNA replication and encapsidation. The study also highlights the importance of the L–P interaction in the polymerase function and provides a structural model for RNA replication in nsNSVs. The findings contribute to the understanding of the structure-function properties of nsNSV polymerases and provide a more complete picture of the different conformations that the polymerase can adopt. The study also provides a potential novel avenue for antiviral drug design by targeting the polymerase dimer interface.