Voltage gated proton channels are strongly inhibited by Zn²⁺, which binds to histidine (His) residues. However, in a molecular model based on similarity between proton channels and the voltage sensing domain of K⁺ channels, the two externally accessible His are too far apart to coordinate Zn²⁺. In view of the proton channel existing as a dimer, we hypothesize that a high affinity Zn²⁺ binding site is created at the dimer interface by His residues from both monomers. Consistent with this idea, Zn²⁺ effects are weaker on monomeric channels. In addition, monomeric channels opened exponentially, and dimeric channels opened sigmoidally, suggesting a Hodgkin-Huxley type process in which multiple subunits undergo a conformational change that precedes opening. This is surprising, because each monomer is thought to contain a separate conduction pathway. Monomeric channel gating had twice weaker temperature dependence than dimeric channels, consistent with a more complex gating mechanism in the dimer. Finally, monomeric channels opened 6.6 times faster than dimeric channels. Combined, these observations suggest that the native proton channel is a dimer in which the two monomers are closely apposed and interact during a cooperative gating process.