Life-history trade-offs between reproduction and survival are well documented, yet the biological mechanisms underlying costs remain unclear. Telomere length (TL) is a potential biomarker for such costs, although its association with reproductive efforts is mixed. Bats, particularly the long-lived greater horseshoe bat ( Rhinolophus ferrumequinum ), provide a rare opportunity to explore these dynamics due to their longevity and low reproductive rates. We examined telomere dynamics in 202 female R. ferrumequinum (819 samples) from a wild population with over 65 y of monitoring, to assess whether reproductive effort leads to telomere shortening (cost of reproduction) or whether longer telomeres were associated with greater reproductive success (reflecting individual quality). Using Bayesian models, we show that females breeding from 2 y of age had significantly shorter relative TL (rTL) compared to females delaying reproduction until later ages. Selective disappearance was evident, with individuals possessing shorter rTL less likely to persist in the population. Cumulative reproductive success showed a positive nonsignificant association with rTL, consistent with the idea that long-term costs may be mitigated by individual quality or selective disappearance of low-quality individuals. However, short-term reproductive costs were evident, particularly in older females that bred in the previous year. Female R. ferrumequinum rTL declined during annual summer reproductive periods, particularly through the energetically demanding lactation stage. Within individuals, shorter rTL was associated with a reduced probability of surviving to the following year. These findings highlight the interplay between reproductive investment, telomere dynamics, and survival, supporting aspects of both the cost of reproduction and individual quality hypotheses in long-lived, low-fecundity species such as bats.