The ends of linear chromosomes are composed of repetitive hexameric sequences called telomeres. Because canonical DNA polymerases cannot fully replicate the ends of linear chromosomes, they shorten with each cycle of replication. Once telomeres become critically short, cells stop replicating and enter a state of replicative arrest--senescence. In this way, telomere length limits the replicative potential of all cells. The enzyme telomerase can maintain telomere length by adding de novo telomeric repeats via reverse transcription from an associated RNA template. Although telomerase expression is exclusive to human somatic and germ stem cells, its expression in somatic stem cells is not sufficient to prevent telomere erosion. Therefore, telomeres shorten with age, effectively serving as a mitotic clock. As in mammals, components of the C. elegans 9-1-1 (HPR-9/MRT-2/HUS-1) DNA damage response complex and its clamp loader, HPR-17, are necessary for telomerase-mediated telomere repeat addition in vivo. Here we present the mapping and characterization of three new telomerase-defective alleles of mrt-2, hpr-17, and hpr-9, and a mutation in a novel gene, all of which possess defects in repairing ionizing radiation- and interstrand crosslink-induced DNA damage. In addition to telomerase, several canonical telomere-binding proteins and other associated proteins maintain telomere length homeostasis and protect chromosome ends from exacerbated erosion and erroneous DNA damage responses in humans. C. elegans harbors four homologs of the human Protection of Telomeres 1 (POT1) telomere capping protein, POT-1, POT-2, POT-3 and MRT-1. Here I identify POT-1 and POT-2 as negative regulators of telomerase-mediated telomere repeat addition in vivo. I demonstrate that POT-1, but not POT-2, protects telomeres from exacerbated erosion. I employ several biochemical strategies to assess whether POT-1 or POT-2 interact with telomerase in vivo. Although an epitope-tagged pot-1 transgene rescued the telomere elongation phenotype of the pot-1 mutant, it exacerbated the onset of senescence in mutants defective for telomerase-mediated telomere repeat addition. We suggest that alterations in telomere capping proteins may drive telomere dysfunction in telomerase-negative cells, which may help to define causal mutations for patients suffering from diseases of premature aging with undefined etiologies.