Telomere maintenance is essential for genome stability, and its regulation during the cell cycle remains a critical area of research. Screening for telomerase-interacting proteins is crucial for understanding the biological processes of telomerase maturation, processing, and recruitment. Using PhastID screening with TERT during S-phase, we identify STRBP, a GEMs-associated protein, as a novel regulator of telomerase activity and telomere length. Our data demonstrate that STRBP mediates interaction with telomerase through TERRA, this interaction negatively regulates telomerase activity, thereby limiting telomere elongation. Notably, TERRA levels decrease during S-phase, potentially facilitating the recruitment of telomerase to telomeres and enabling telomere extension.