Although the effects of prenatal under-nutrition on adult cardiovascular health have been well studied, its effects on the cerebrovascular structure and function remain unknown. We used a pair-fed rat model of 50% caloric restriction from day 11 of gestation to term, with ad libitum feeding after birth. We validated that maternal food restriction (MFR) stress is mediated by glucocorticoids by administering Metyrapone, a corticosterone synthesis inhibitor, to MFR mothers at day 11 of gestation. At age 8-months, Control, MFR, and MFR+Metyrapone offspring were sacrificed and middle cerebral artery (MCA) segments were studied using vessel-bath myography and confocal microscopy. Colocalization of smooth muscle α-actin (SMαA) with non-muscle (NM), SM1 and SM2 myosin heavy chain (MHC) isoforms was used to assess smooth muscle phenotype. Our results indicate that artery stiffness and wall thickness were increased, pressure-evoked myogenic reactivity was depressed, and myofilament Ca⁺⁺ sensitivity was decreased in MFR compared to Control offspring. MCA from MFR offspring exhibited a significantly greater SMαA/NM colocalization, suggesting that the SMC's had been altered toward a non-contractile phenotype. MET significantly reversed the effects of MFR on stiffness but not myogenic reactivity, lowered SMαA/NM colocalization, and increased SMαA/SM2 colocalization. Together, our data suggest that MFR alters cerebrovascular contractility via both glucocorticoid-dependent and glucocorticoid-independent mechanisms.