Telomeres are chromosome protectors that shorten during cell replication and in stressful conditions. Developing individuals are susceptible to telomere erosion when their growth is fast and resources limited. This is critical because the rate of telomere attrition in early life is linked to health and life span of adults. The metabolic telomere attrition hypothesis (MeTA) suggests that telomere dynamics can respond to biochemical signals conveying information about the organism’s energetic state. Among these signals are glucocorticoids (hormones that promote catabolic processes, potentially impairing costly telomere maintenance) and nucleotides, which activate anabolic pathways though the cellular enzyme target of rapamycin (TOR) preventing telomere attrition. During the energetically demanding growth phase, the regulation of telomeres in response to two contrasting signals—one promoting telomere maintenance and the other inducing attrition—provides an ideal experimental setting to test MeTa. We studied nestlings of a rapidly developing free-living passerine, the great tit (Parus major), that either received glucocorticoids (Cort-chicks), nucleotides (Nuc-chicks), or a combination of both (NucCort-chicks) all compared with controls (Cnt-chicks). Contrary to Cort-chicks, which showed telomere attrition, NucCort-chicks, did not. NucCort-chicks was the only group showing increased gene expression of telo2 (proxy for TOR activation), of mitochondrial enzymes linked to ATP production (atp5f1a-atp5f1b-cox6a1-cox4) and a higher efficiency in aerobically producing ATP. NucCort-chicks had also a higher expression of telomere maintenance genes (trf2) and of enzymatic antioxidant genes (gpx4-sod1). The findings show that nucleotides availability is crucial for preventing telomere erosion during fast growth in stressful environments.