Much of the centrally available oxytocin (OT) is synthesized in magnocellular neurons located in the paraventricular nucleus of the hypothalamus. This same area is home to parvocellular corticotropin-releasing hormone (CRH) synthesizing neurons that regulate activation of the hypothalamic-pituitary-adrenal (HPA) axis. A large body of data indicates that complex interactions between these systems inextricably link central OT signaling with the neuroendocrine response to stress. This review focuses on a small but diverse set of cellular and synaptic mechanisms that have been proposed to underlie intrahypothalamic OT/CRF interactions during the response to acute stress.