Understanding ageing and the diversity of life histories is a cornerstone in biology. Telomeres, the protecting caps of chromosomes, are thought to be involved in ageing, cancer risks and life‐history strategies. They shorten with cell division and age in somatic tissues of most species, possibly limiting lifespan. The resource allocation trade‐off hypothesis predicts that short telomeres have thus coevolved with early reproduction, proactive behaviour and reduced lifespan, that is, a fast pace‐of‐life syndrome (POLS). Conversely, since short telomeres may also reduce the risks of cancer, the anticancer hypothesis advances that they should be associated with slow POLS. Conclusion on which hypothesis best supports the role of telomeres as mediators of life‐history strategies is hampered by a lack of study on wild short‐lived vertebrates, apart from birds. Using seven years of data on wild Eastern chipmunks Tamias striatus, we highlighted that telomeres elongate with age (n = 204 and n = 20) and do not limit lifespan in this species (n = 51). Furthermore, short telomeres correlated with a slow POLS in a sex‐specific way (n = 37). Females with short telomeres had a delayed age at first breeding and a lower fecundity rate than females with long telomeres, while we found no differences in males. Our findings support most predictions adapted from the anticancer hypothesis, but none of those from the resource allocation trade‐off hypothesis. Results are in line with an increasing body of evidence suggesting that other evolutionary forces than resource allocation trade‐offs shape the diversity of telomere length in adult somatic cells and the relationships between telomere length and life‐histories.