Previous studies implicate the hypothalamic ventromedial nucleus (VMN) in glycemic control. Here, we report that selective inhibition of the subset of VMN neurons that express the transcription factor steroidogenic-factor 1 (VMN^SF1 neurons) blocks recovery from insulin-induced hypoglycemia whereas, conversely, activation of VMN^SF1 neurons causes diabetes-range hyperglycemia. Moreover, this hyperglycemic response is reproduced by selective activation of VMN^SF1 fibers projecting to the anterior bed nucleus of the stria terminalis (aBNST), but not to other brain areas innervated by VMN^SF1 neurons. We also report that neurons in the lateral parabrachial nucleus (LPBN), a brain area that is also implicated in the response to hypoglycemia, make synaptic connections with the specific subset of glucoregulatory VMN^SF1 neurons that project to the aBNST. These results collectively establish a physiological role in glucose homeostasis for VMN^SF1 neurons and suggest that these neurons are part of an ascending glucoregulatory LPBN→VMN^SF1→aBNST neurocircuit.