Lifetime reproductive success (LRS) is what counts in terms of evolution, but investments in reproduction entail costs for an organism. The idea that telomere dynamics may be shaped in response to such costs is already established, however we still lack information if this relation translates to overall fitness. Here, we quantified lifetime reproductive success (number of fledged young) and longitudinal telomere dynamics of small passerine birds - the blue tits. We found that individual telomere erosion rate was positively associated with lifetime fledgling number. Birds with more fledged young experienced increased telomere attrition. We show that telomere attrition rate, but not telomere length, is related to individual fitness and suggest that telomere dynamics may underlie reproductive costs experienced by animals as a consequence of prioritizing their lifetime fitness. This is the first study to provide evidence that more pronounced telomere erosion is associated with higher fitness gain.