Key points  The nociceptin/ORL1 receptor neuropeptide system is related to opioid systems and thought to be involved in pain modulation. A major mechanism of action of this system is inhibition of calcium channels that control excitability of sensory nerves. To understand the potential for drugs acting on this system to modulate pain it is important to identify the types of sensory nerve cells functionally expressing the ORL1 receptor and how they are modulated. Here we identified a subpopulation of small, presumably pain sensing sensory nerves that are highly responsive to this neuropeptide both in their cell bodies and nerve terminals. We then established that nociceptin/ORL1 stimulation inhibits calcium channels only while the peptide is present on the cells or their nerve terminals but does not produce long‐term down‐regulation of calcium channel function as had been previously proposed.