Changes in telomere dynamics could underlie life-history trade-offs among growth, size and longevity, but our ability to quantify such mechanistic processes in natural, unmanipulated populations is limited. We investigated how 4 years of artificial selection for either larger or smaller body size affected early-life telomere length in two insular populations of wild house sparrows. A negative correlation between telomere length and structural size was evident under both selection regimes. The study also revealed that male sparrows had longer telomeres than females, after controlling for size, and there was a significant negative effect of harsh weather conditions on telomere length. The long-term fitness consequences of these changes in early-life telomere length induced by the artificial size selection were explored over a period of 11 years. These analyses indicated disruptive selection on telomere length because both short and long early-life telomere length tended to be associated with the lowest mortality rates and highest life expectancy. There was also weak evidence for a negative association between telomere length and annual reproductive success, but only in the population where body size was increased experimentally. Our results suggest that natural selection for optimal body size in wild animals will affect early-life telomere length during growth, which is known to be linked to longevity in birds, but also that the importance of telomeres for long-term somatic maintenance and fitness is complex in a wild bird species.