Transient receptor potential vanilloid 1 (TRPV1) is a Ca2+ permeable non‐selective cation channel activated by physical and chemical stimuli. Resiniferatoxin (RTX), an ultrapotent agonist of TRPV1, is under investigation for treatment of urinary bladder hyper‐reflexia and chronic pain conditions. Here, we have determined the characteristics of RTX‐induced responses in cells expressing native and cloned rat TRPV1. Whole‐cell currents increase with repeated application of submaximal concentrations of RTX until a maximal response is attained and do not deactivate even after prolonged washout. Interestingly, the rate of activation and block by capsazepine of RTX‐induced currents are significantly slower than for capsaicin‐induced currents. RTX‐induced whole‐cell currents are outwardly rectifying, but to a lesser extent than capsaicin‐induced currents. RTX‐induced single channel currents exhibit multiple conductance states and outward rectification. The open probability (Po) of RTX‐induced currents is higher at all potentials as compared to capsaicin‐induced currents, which showed a strong voltage‐dependent decrease at negative potentials. Single‐channel kinetic analyses reveal that open‐time distribution of RTX‐induced currents can be fitted with three exponential components at negative and positive potentials. The areas of distribution of the longer open time constants are significantly larger than capsaicin‐induced currents. The closed‐time distribution of RTX‐induced currents can be fitted with three exponential components as compared to capsaicin‐induced currents, which require four exponential components. Current‐clamp experiments reveal that low concentrations of RTX caused a slow and sustained depolarization beyond threshold while generating few action potentials. Concentrations of capsaicin required for the same extent of depolarization generated a significantly greater number of action potentials. These properties of RTX may play a role in its clinical usefulness.