Cranial visceral afferents contact neurons within the solitary tract nucleus (NTS) and evoke homeostatic reflex pathways. Descending projections from the paraventricular nucleus (PVN) of the hypothalamus release oxytocin to modulate visceral afferent communication with NTS neurons. However, the mechanisms through which oxytocin acts are poorly understood. From male Sprague-Dawley rats, horizontal brainstem slices containing the solitary tract (ST) and medial NTS were isolated under deep isoflurane anesthesia (5% by inhalation). Brain slices were maintained in physiological bath (34°C, 95% O₂/5% CO₂ bubbled) and whole-cell patch clamp recordings were made under voltage clamp. Remote electrical shocks to afferent axons in the ST produced highly consistent glutamatergic excitatory postsynaptic currents (EPSCs) (jitter of < 200 μs) and identified NTS neurons receiving direct ST afferent innervation. Oxytocin increased the amplitude of ST-evoked EPSCs (131 ± 12% at 1000 nM, n = 3) with no effect on event kinetics. Variance-mean analysis of ST-evoked EPSCs, under varying calcium concentrations, indicates oxytocin increases the release probability of glutamate (control: 57 ± 3% vs. oxytocin: 80 ± 10%, n = 3) from the afferent terminals suggestive of a presynaptic site of action. Glutamate mediated miniature EPSCs (mEPSCs) were isolated through blocking action potential transmission with tetrodotoxin and the GABA_A receptor antagonist gabazine (SR-95531). Oxytocin increased the frequency of mEPSCs (159 ± 9%, 202 ± 19% at 100 nM, 1000 nM oxytocin, n = 5-8 neurons) but had no effect on the event kinetics. The oxytocin receptor antagonist (d(CH2)51,Tyr(Me)2,Thr4,Orn8,des-Gly-NH29-Vasotocin) blocked this effect on mEPSCs. In addition, oxytocin (1000 nM) evoked an inward holding current (13 ± 3 pA, n = 5); consistent with postsynaptic modulation of ion channels. Taken together these findings suggest oxytocin released from PVN projections may enhance glutamatergic visceral afferent transmission within NTS via both pre- and postsynaptic sites of action.