The ends of linear eukaryotic chromosomes shorten with each cell cycle due to the end-replication problem, ultimately leading to senescence and death. Telomerase countervails this deficiency by synthesizing telomeric repeats by reverse transcribing a portion of its RNA subunit, thus providing cell proliferation potential, critical to aging and cancer. It has become apparent that telomerase provides telomere-length homeostasis by preferentially extending the shortest ends. However, it is not clear how this selective telomerase action is achieved. One major mechanism by which telomerase is regulated is its recruitment to telomeres. In S. cerevisiae, two subunits of the RNA-protein enzyme have been shown to be involved in recruitment: Est1 recruits telomerase to the telomeric end-binding protein Cdc13, whereas Ku recruitment was also known to occur, but it was not clear how. We have determined that telomerase recruitment by Ku requires the interacting protein, Sir4, which is an integral part of telomeric silent chromatin. Epistasis analysis puts Ku, Sir4 and the Ku-binding site of telomerase RNA, TLC1, in the same pathway. Additionally, we were able to bypass Ku in telomerase recruitment and telomere length regulation by tethering telomerase RNA directly to Sir4. Having established the Ku-Sir4 recruitment pathway, we then evaluated its role in telomere length regulation. Introducing multiple Ku-binding sites in telomerase RNA caused telomere hyperlengthening, demonstrating the acute sensitivity of telomere length to the Ku-mediated telomerase recruitment pathway. This phenotype reminded us of the runaway-telomeres of rif1∆ and rif2∆ mutants and since Rif proteins also directly compete with Sir4 for binding to the telomeric double-stranded DNA binding protein Rap1, we tested if hyperelongated telomeres in rif∆ mutants require Ku function in telomerase. We found that nearly wild-type telomere length returns to rif∆ cells upon deletion of the Ku-binding hairpin in TLC1. These results suggest that direct interplay between Rif and Sir4 proteins along the distal portions of chromosomes is key to sensing telomere length and, in turn, appropriately recruiting telomerase preferentially to the shortest telomeres.