Physiologic actions of insulin via activation of the PI3 kinase/Akt pathway in the endothelium serve to couple regulation of hemodynamic and metabolic homeostasis. Insulin resistance, endothelial dysfunction, and hypertension increase in prevalence with aging. We investigated the metabolic and endothelial actions of insulin in 24-month vs. 3-month Sprague Dawley rats. Using the hyperinsulinemic euglycemic clamp, the rate of glucose infusion necessary to maintain equivalent plasma glucose (5.5mmol/L) was similar in 24-month vs. 3-month, as was fasting glucose (5.2±0.33 vs. 4.4±0.37mmol/L; mean±SEM) and insulin (0.862±0.193 vs. 1.307±0.230mg/L). Systolic blood pressure was higher in 24-month (133±5 vs.110±4; P=0.005). Endothelial nitric oxide (NO)-dependent relaxation to insulin was impaired in aortas of 24-month vs. 3-month (Emax 8.9±4.3% vs. 34.9±3.9%; P=0.002); L-NAME abolished insulin-mediated relaxation in 3-month but not 24-month. Endothelium NO-dependent (acetylcholine) and independent (sodium nitroprusside) relaxation as well as NADPH oxidase activity were similar in 3- and 24-month. Insulin increased aortic serine phosphorylation of Akt in 3-month by 120% over 24-month (P<0.05) and serine phosphorylation of eNOS in 3-month by 380% over 24-month (P<0.05). Aortic expression of phosphorylated JNK1 and serine phosphorylated IRS-1, known mediators of metabolic insulin resistance, was similar in 3- and 24-month. Expression of caveolin-1, a regulator of eNOS activity and insulin signaling, was 55% lower in 24-month than 3-month (P=0.002). In summary, impaired vasorelaxation to insulin in aging was independent of metabolic insulin sensitivity and associated with impaired insulin-mediated activation of the Akt/eNOS pathway, but intact activation of the acetylcholine-mediated Ca²⁺-calmodulin/eNOS pathway. Vascular insulin resistance in aging may add to the increased susceptibility of this population to vascular injury induced by traditional cardiovascular risk factors.