Transcriptional elongation by RNA polymerase II (RNAPII) is regulated by the positive transcription elongation factor b (P-TEFb), which contains Cdk9 and a C-type cyclin (CycT1, CycT2a, CycT2b, or CycK). Whereas their N-terminal cylin boxes are almost identical, the C-terminal sequences of CycT1 and CycT2 are divergent. Previously, a histidine-rich stretch in CycT1 was found to bind the CTD of RNAPII and direct the transcriptional activity of this P-TEFb complex when tethered artificially to DNA. The global repressor PIE-1 from C. elegans blocked its effects. In this study, C-terminal truncations of CycT2 past its histidine-rich stretch, to a leucine-rich region next to its cyclin boxes, still maintained appreciable transcriptional activity. Moreover, this domain bound RNAPII via its CTD and PIE-1 blocked its effects. Thus, CycT2 not only contains two domains that target RNAPII but this substrate recognition is necessary for its transcriptional activity via DNA.