Summary Telomeres of most species are simple repetitive sequences that are maintained by de novo telomere repeat addition by the ribonucleoprotein telomerase. Small RNAs composed of perfect telomere repeats have been observed in several organisms, but their functions are not well understood. We discovered an endogenous C. elegans small RNA pathway that promotes telomere stability in the absence of telomerase. C. elegans small RNAs that are perfectly complementary to telomeric DNA are very rare, measuring 1 read per 10 million small RNAs. However, two related Caenorhabditis species, C. briggsae and C. remanei, have telomeric small RNA levels that are increased by several orders of magnitude. Telomeric small RNAs in all three Caenorhabditis species are strongly depleted for 5' guanine nucleotides that characterize major C. elegans small RNA species like 26G and 22G RNAs. Together, these results suggest that telomeric small RNAs have a distinct biogenesis mechanism and that a dramatic change in their role at telomeres may have occurred during recent Caenorhabditis evolution. We propose to study the relationship between small RNAs and telomere biology in these Caenorhabditis species, in an effort to understand what regulates telomeric small RNA abundance, how telomeric small RNAs are created, and what their functions are. Potentially analogous telomeric small RNAs have been observed in ciliates and mammals, and we may help to elucidate their biological relevance.