Telomere length variation has been implicated in processes of ecological and evolutionary importance in a wide range of organisms. However, while the temporal component of this variation has been the subject of much research, we do not know yet whether a spatial component exists within species in telomere dynamics. Here, we investigated for the first time whether the biogeographic history of populations, a key driver of eco-evolutionary processes, can influence telomere dynamics. Based on a one-year longitudinal common-garden experiment in a tree frog species we found that co-specific populations can show striking differences in telomere dynamics, not explained by distinct environmental conditions experienced by individuals through time. Indeed, the populations did not differ in telomere length at the beginning of the study, yet they did after one year under standard conditions. We observed stability of telomere length over time within historically stable populations, but remarkable elongation (31.2% on average) within populations arisen during a recent range expansion. Our results suggest the intriguing scenario that non-equilibrium processes, such as range expansions, might promote plasticity in the molecular machinery regulating telomere dynamics.