Influenza virus RNA polymerase (FluPol), a heterotrimer composed of PB1, PB2, and PA subunits (P3 in influenza C), performs both transcription and replication of the viral RNA genome. For transcription, FluPol interacts with the C-terminal domain (CTD) of RNA polymerase II (Pol II), which enables FluPol to snatch capped RNA primers from nascent host RNAs. Here, we describe the co-crystal structure of influenza C virus polymerase (FluPolC) bound to a Ser5-phosphorylated CTD (pS5-CTD) peptide. The position of the CTD-binding site at the interface of PB1, P3, and the flexible PB2 C-terminal domains suggests that CTD binding stabilizes the transcription-competent conformation of FluPol. In agreement, both cap snatching and capped primer-dependent transcription initiation by FluPolC are enhanced in the presence of pS5-CTD. Mutations of amino acids in the CTD-binding site reduce viral mRNA synthesis. We propose a model for the activation of the influenza virus transcriptase through its association with pS5-CTD of Pol II. Display omitted •Influenza C virus RNA polymerase binds the CTD of RNA polymerase II•Pol II CTD binding allows the viral polymerase to snatch capped RNA primers•Pol II CTD binding stabilizes the transcriptase conformation of the viral polymerase•Pol II CTD binding enhances viral transcription The influenza virus RNA polymerase acts both as transcriptase and replicase. Serna Martin et al. solve the structure of the influenza C virus polymerase bound to a peptide mimicking the C-terminal domain of Pol II and demonstrate that binding to Pol II stabilizes the transcriptase conformation of the viral polymerase.