The six-protein shelterin complex safeguards mammalian chromosome ends, however, its intricate protein-protein and protein-DNA interactions complicate biochemical dissection. The C. elegans DNA-binding TEBP-1/2 (also known as DTN-1/2) and POT-1 proteins directly interact, offering a simplified system to dissect chromosome end protection. Here, we combined protein crystallography with in vivo functional analyses to elucidate the architecture and assembly of the C. elegans telomere-binding protein complex. We uncover a striking interface in which the canonical single-stranded DNA-binding OB domain of POT-1 is repurposed to engage TEBP-1/2, rewiring telomeric protein connectivity. Disruption of the electrostatic interfaces between POT-1 and TEBP-1/2 disassembles the complex in vivo and causes telomere hyper-elongation. POT-1 OB retains binding to the 5′-phosphorylated end of the telomeric ds-ssDNA junction, a role required for robust telomeric localization of POT-1 and suppression of telomere hyper-elongation in vivo. Together, our findings support a model in which TEBP-1/2 recruit POT-1 to form a three-way TEBP-1/2–POT-1–DNA junction complex that ensures telomere length homeostasis.