Telomeres are DNA structures that protect chromosome ends. However, telomeres shorten during cell replication and at critically low lengths can reduce cell replicative potential, induce cell senescence and decrease fitness. Stress exposure, which elevates glucocorticoid hormone concentrations, can exacerbate telomere attrition. This phenomenon has been attributed to increased oxidative stress generated by glucocorticoids ("oxidative stress hypothesis"). We recently instead suggested that glucocorticoids increase telomere attrition during stressful periods by reducing the resources available for telomere maintenance through changes in the metabolic machinery ("metabolic telomere attrition hypothesis"). Here we tested whether experimental increases in glucocorticoid levels affected telomeres and mitochondrial function in wild great tit (Parus major) nestlings during the energy-demanding early growth. We monitored resulting corticosterone (Cort) concentrations in plasma, and in red blood cells telomere lengths and mitochondrial metabolism (metabolic rate, proton leak, oxidative phosphorylation, maximal mitochondrial capacity and mitochondrial inefficiency). We assessed oxidative damage caused by reactive oxygen species (ROS) metabolites as well as the total non-enzymatic antioxidant protection in plasma. Compared with control (Ctrl) nestlings, Cort-nestlings had higher baseline corticosterone, shorter telomeres and higher mitochondrial metabolic rate. Importantly, Cort-nestlings showed increased mitochondrial proton leak, leading to a decreased ATP production efficiency. Treatment groups did not differ in oxidative damage or antioxidants. Hence, glucocorticoid-induced telomere attrition is associated with changes in mitochondrial metabolism, but not with ROS production. These findings support the "metabolic telomere attrition hypothesis" which proposes an active regulation of telomere length by glucocorticoids during stressful periods, which is mediated through metabolic rearrangements.