Telomerase reverse transcriptase (TERT) and telomerase RNA (TER) function together to create a uniquely specialized polymerase. Here we have described for the first time domains of bacterially expressed Tetrahymena TERT that interacted directly with TER in the absence of assembly chaperones. We used quantitative binding assays to define TER sequence requirements for recognition by the high affinity RNA binding domain and an independent N-terminal RNA interaction domain. The TERT RNA binding domain and N-terminal RNA interaction domain had distinct, nonoverlapping requirements for TER sequence and structure that together accounted for all of the sites of TER contact inferred for full-length TERT. The TER residues important for TERT binding are only a subset of the residues required for catalytic activity. Our findings demonstrate telomerase functional specialization by an elaborate ribonucleoprotein architecture physically separable from the active site.