The M2 protein of the influenza virus conducts protons into the virion under external acidic pH. The proton selectivity of the tetrameric channel is controlled by a single histidine (His37), whereas channel gating is accomplished by a single tryptophan (Trp41) in the transmembrane domain of the protein. Aromatic interaction between these two functional residues has been previously observed in Raman spectra, but atomic-resolution evidence for this interaction remains scarce. Here we use high-resolution solid-state NMR spectroscopy to determine the side-chain conformation and dynamics of Trp41 in the M2 transmembrane peptide by measuring the Trp chemical shifts, His37-Trp41 distances, and indole dynamics at high and low pH. The interatomic distances constrain the Trp41 side-chain conformation to trans for χ1 and 120–135° for χ2. This t90 rotamer points the Nε1-Cε2-Cζ2 side of the indole toward the aqueous pore. The precise χ1 and χ2 angles differ by ∼20° between high and low pH. These differences, together with the known changes in the helix tilt angle between high and low pH, push the imidazole and indole rings closer together at low pH. Moreover, the measured order parameters indicate that the indole rings undergo simultaneous χ1 and χ2 torsional fluctuations at acidic pH, but only restricted χ1 fluctuations at high pH. As a result, the Trp41 side chain periodically experiences strong cation-π interactions with His37 at low pH as the indole sweeps through its trajectory, whereas at high pH the indole ring is further away from the imidazole. These results provide the structural basis for understanding how the His37-water proton exchange rate measured by NMR is reduced to the small proton flux measured in biochemical experiments. The indole dynamics, together with the known motion of the imidazolium, indicate that this compact ion channel uses economical side-chain dynamics to regulate proton conduction and gating.