The paraventricular nucleus (PVN) of the hypothalamus is important in maintaining homeostasis and can alter cardiovascular function via autonomic control, however, the mechanisms underlying this control are not fully understood. PVN neurones are home to a wide array of ion channels and we have previously reported coupling between TRPV4 and small-conductance calcium-activated potassium channels (SK) to facilitate osmosensing in the PVN [1]. The PVN is also known to have thermoregulatory roles, therefore, we investigate whether TRPV4 may play a role in thermosensing. To characterise single-channel gating of TRPV4 and spontaneous action current firing from parvocellular PVN neurones, we used patch-clamp electrophysiology on mouse hypothalamic brain slices. Heart rate, blood pressure and tail blood volume were recorded from CD1 mice using non-invasive tail plethysmography. Results are given as mean±SEM, statistical significance was assessed by ANOVA or Student’s t-tests as appropriate. We identified a TRPV4-like channel on parvocellular PVN neurones with a conductance of 59.7±1 pS and Vrev of −5.9±3 mV (n=9) that was sensitive to the TRPV4 inhibitor GSK2193874. When temperature was increased, we observed a dramatic increase in open probability (Po), from 0.19±0.07 at 22°C to 0.54±0.07 at 32°C and 0.82±0.07 at 37°C, which was mediated by profound increases in the mean open durations (n=9,**p< 0.01,***p<0.001). A NEURON model, adapted from Feetham et al., (2015) [1] but with temperature dependent stochastic gating of TRPV4, and secondary Ca2+-dependent activation of SK channels, predicted that action potential frequency of these neurones would decrease with temperature. This was confirmed with action current frequency (Apf) measurements from parvocellular PVN neurones. Apf decreased when temperature was increased from 22°C to 37°C (**p<0.001, n=6). This effect was inhibited at temperatures up to 32°C by the broad-spectrum channel blocker gadolinium (100 µM) but not at physiological temperatures (37°C). In the presence of the TRPM2 blocker Econazole (10 µM), the effect was inhibited at all temperatures, indicating a role also for TRPM2 in thermosensing in the PVN. In whole animal experiments, inhibition of TRPV4 (GSK2193874, 300 µg/kg, i.p) resulted in an increased tail blood volume response to ambient heat application (>33°C), which was not observed in control (n=4, **p<0.01). Our data shows that TRPV4-like channels on mouse parvocellular PVN neurones are sensitive to temperature change; increasing temperature has profound effects on channel gating. We postulate that TRPV4 channels on the PVN may be involved in thermosensing and show that pharmacological inhibition of TRPV4 results in an increased temperature evoked vasodilation response in mice. Our spontaneous action current data, however, suggests that the temperature sensing in the PVN is complex, and is likely mediated by an interplay of multiple channel subtypes, including TRPV4 and TRPM2.