Pregnancy increases sympathetic nerve activity, but the mechanisms are unknown. Here, we investigated the contributions of the hypothalamic paraventricular and arcuate nuclei in α-chloralose-anesthetized pregnant and nonpregnant rats. Baseline arterial pressure was lower, and heart rate, lumbar sympathetic activity and splanchnic sympathetic nerve activity were higher in pregnant compared to nonpregnant rats. Inhibition of the paraventricular nucleus via bilateral muscimol nanoinjections decreased arterial pressure more in pregnant than nonpregnant rats, and decreased heart rate and lumbar sympathetic nerve activity only in pregnant rats. Similarly, following arcuate muscimol nanoninjections, the decreases in arterial pressure, heart rate, and lumbar, renal, and splanchnic sympathetic nerve activities, were greater in pregnant than nonpregnant rats. Major arcuate neuronal groups that project to the paraventricular nucleus express inhibitory Neuropeptide Y and excitatory α-melanocyte stimulating hormone. Inhibition of paraventricular melanocortin 3/4 receptors with SHU9119 also decreased arterial pressure, heart rate, and lumbar sympathetic nerve activity in pregnant, but not nonpregnant rats. Conversely, paraventricular nucleus Neuropeptide Y expression was reduced in pregnant animals, and while blockade of paraventricular Neuropeptide Y Y1 receptors increased arterial pressure, heart rate, and lumbar sympathetic activity in nonpregnant rats, it had no effects in pregnant rats. Yet, the sympathoinhibitory, depressor and bradycardic effects of Neuropeptide Y nanoinjections were similar between groups. In conclusion, the paraventricular and arcuate nuclei contribute to increased basal sympathetic nerve activity during pregnancy, likely due in part to decreased tonic Neuropeptide Y inhibition and increased tonic α-melanocyte stimulating hormone excitation of presympathetic neurons in the paraventricular nucleus.