Intrauterine growth restriction (IUGR) of the placenta and fetus affects approximately 8% of all pregnancies and is associated with short- and long-term metabolic complications. In pregnant sheep, environmental heat stress causes placental growth restriction and lowers its functional capacity. The inadequate oxygen and nutrient supply to the fetus leads to IUGR and provokes an endocrine stress response that raises concentrations of catecholamines during late gestation. We propose that sustained high norepinephrine concentrations produce developmental adaptations in insulin secretion and action. The effects of sustained high catecholamines in IUGR fetuses created by hyperthermia-induced placental insufficiency were determined during an acute pharmacological blockade of adrenergic receptors and in fetuses with a bilateral adrenal demedullation (AD). Glucose-stimulated insulin secretion and insulin sensitivity was also measured in IUGR and control lambs. Placental mass was lower at 103 and 134 days of gestation, but significant reductions in fetal weights were only observed at 134 days (term 149 days). IUGR fetuses had lowered oxygen, glucose, and insulin concentrations at 103 and 134 days. Plasma norepinephrine concentrations were 3-5 fold higher in IUGR fetuses compared to controls. Glucose-stimulated insulin concentrations were increased in IUGR fetuses during the adrenergic blockade at both gestational ages, which indicates adrenergic inhibition of insulin secretion but also identifies a compensatory gain of function because β-cell mass was substantially lower than controls. To determine the impact of sustained hypercatecholaminemia, IUGR and control fetuses underwent a sham (intact) or AD surgical procedure at 98 days. At 134 days, AD-IUGR fetuses had lower norepinephrine concentrations than intact-IUGR fetuses despite being hypoxemic and hypoglycemic. Glucose-stimulated insulin concentrations were greater in AD-IUGR fetuses compared to intact-IUGR fetuses, and similar to AD-controls, but all treatments were lower than intact-controls. Together, these data show that high norepinephrine concentrations inhibit insulin secretion persistently in IUGR fetuses, but chronic adrenergic stimulation creates a compensatory gain in function. This augmentation in insulin secretion persisted in 8 day old IUGR lambs. In addition, insulin sensitivity for glucose utilization was greater in IUGR fetuses and lambs. Moreover, at 103 days the glucose-to-insulin ratio was greater in IUGR fetuses than control fetuses, but during the adrenergic blockade the ratio was not different than control fetuses. Hyperinsulinemic-euglycemic clamps were performed in lambs at 15 days and glucose disposal rates determined with radiolabeled glucose show that IUGR lambs have greater insulin sensitivity compared to control lambs in unstimulated and hyperinsulinemic steady state periods. Therefore, fetal stress due to placental insufficiency elevates catecholamines chronically to spare the fetus by inhibiting insulin while maintaining glucose utilization rates. However, the compensatory actions in young lambs create an imbalance between insulin secretion and insulin sensitivity that may promote a loss of function as the insulin disposition index is corrected.