Globally, the prevalence of diabetic kidney disease (DKD) continues to rise at an alarming rate and is a major risk factor for premature death. Early age at diabetes diagnosis exacerbates the risk for DKD, with most adult therapies having fewer benefits in youth, but there is a lag in the molecular understanding of this in humans. Here we show that mitochondrial dysfunction is present in youth with high DKD risk and that a mitochondrial therapy (MitoTx) targeting this pathway may be efficacious. Firstly, we demonstrate that mice with a heterozygous mutation in mitochondrial complex I subunit Ndufs6, common in humans (1:250), exhibit impairment in kidney function, as well as proximal tubule and kidney immune cell mitochondrial dysfunction, which are amplified by diabetes and reversed with MitoTx. MitoTx’s therapeutic benefit was confirmed in a second murine model of diabetes and early kidney disease. Secondly, we studied three cohorts of youth with diabetes and varied risk for DKD. In young adults (YA) with type 1 diabetes (T1DM; 20±3 yrs, n=100), recruited in Brisbane, Australia, stratified for future DKD risk (low, uACR<1.17, n=66 vs high, uACR≥1.17 mg/mmol, n=34), greater mitochondrial dysfunction in circulating CD4+T cells, particularly Treg was evident in high-risk individuals using functional ATP production assays, flow cytometry and fuel changes by plasma metabolomics. Human proximal tubule kidney cells exposed to high-risk patient plasma showed mitochondrial defects in both fatty acid β-oxidation and non-fatty acid-derived ATP production. As a predictive biomarker of mitochondrial dysfunction, urine mtDNA:nDNA was associated with greater urinary albumin excretion both in YA and in a second cohort of adolescents (n=80, 14±2 yrs). Finally, we also found a signature of mitochondrial dysfunction in biopsy kidney cells from youth onset diabetes and early DKD (n=6), using previously generated single-cell transcriptomics and gene availability data. Together, these studies postulate that mitochondrial dysfunction is an early and pathological manifestation in human DKD that can be therapeutically targeted and should be evaluated to prevent the onset and progression to overt kidney disease and premature death in people with diabetes.