The proton-activated sodium channel ASIC1 belongs to the ENaC/Degenerins family of ion channels. Little is known about gating of the pore in any member of this class. Here we outline the shape of the ion pathway of ASIC1 in the open and closed conformations by measuring apparent rates of cysteine modification by thiol-specific reagents in the two transmembrane helices that form the pore (TM1 and TM2). Closed channels have a narrowing in the external end of the pore, whereas open channels have a narrowing midway, the length of TM2 that serves as selectivity filter. Thus, gating of the pore entails straightening the tilt of TM2 without significant rotation. The findings imply that the external narrowing serves as opening, closing and desensitization gate, and that the selectivity filter of ASIC1 is a transient structure that assembles in the open state and is pulled apart in the closed state.