Capsaicin, the pungent ingredient of hot peppers, has long been used to identify nociceptors. Its molecular target, the vanilloid receptor VR1, was recently cloned and confirmed functionally as a polymodal detector of multiple pain stimuli: heat, acid, and vanilloids. Previous electrophysiology studies have focused on whole-cell characteristics of the receptor. Here, we provide the first in-depth single-channel kinetic study of VR1 to understand its activation mechanism. At low to medium concentrations, channel activity appeared as bursts. Not only did the durations of the interburst gaps vary with capsaicin, the bursts also appeared ligand-dependent, with high capsaicin prolonging bursts and stabilizing openings. Gating involved at least five closed and three open states, with strong correlations between short closures and long openings, and long closures and short openings. Increasing capsaicin reduced the long closures with little effect on short ones. The open time constants changed little with capsaicin concentration, though their relative proportions varied. These results suggest that 1), the channel contains multiple capsaicin binding sites; 2), both partial and full binding are capable of opening the channel; 3), when activated, multiple open states are accessible irrespective of the level of binding; and 4), capsaicin association occurs preferentially to the closed channel.