Telomeres shorten with age, and telomere length (TL) can predict lifespan. In vitro studies have established that the shortest telomeres in the genome drive cellular senescence, but whether they also drive in vivo lifespan variation is undecided. Moreover, it is not well known to what extent the TL-lifespan association can be attributed to variation in TL per se vs. variation in telomere dynamics prior to sampling. We investigated whether absolute TL, telomere dynamics, or both, serve as predictors of lifespan using longitudinal blood samples from adult captive zebra finches of both sexes that were raised in either small or large broods. We measured TL through telomere restriction fragment analysis, which provides information on the TL distribution within samples in addition to estimates of mean sample TL. Birds with shorter lifespans displayed accelerated telomere shortening and the association between telomere shortening and lifespan was steeper at higher percentiles. Absolute mean TL at any point did not predict lifespan or remaining lifespan and neither brood size nor sex were found to affect TL or telomere dynamics. Collectively, our findings support telomere dynamics—rather than average TL—better predict lifespan, likely more accurately reflecting cumulative physiological stress than TL. This relationship was more pronounced at the longer telomeres in the genome.