Telomerase reverse transcriptase (TERT) differs from many other reverse transcriptases in that it remains stably associated with its template-containing RNA subunit. Elements of TERT involved in binding the RNA subunit have now been identified by mutagenesis and in vitro reconstitution of the Tetrahymena ribonucleoprotein complex. Mutations in the reverse transcriptase motifs of TERT reduced activity as expected but did not greatly reduce its binding to the telomerase RNA. In contrast, all mutations in the T and CP motifs dramatically reduced RNA binding. We therefore suggest that the T and CP motifs of TERT function to hold on to the telomerase RNA, leaving the RNA template region free to translocate through the RT domain.