The chemiosmotic theory postulated that the inner mitochondrial membrane (IMM) is impermeable to K⁺. This abundant cytosolic cation can be attracted into the mitochondrial matrix by the extremely negative voltage, causing uncontrolled mitochondrial swelling, depolarization, and disruption of ATP production. However, the IMM has been proposed to have various mechanisms of K⁺ permeability, ranging from a slow K⁺ uniport to large-conductance K⁺ channels. To resolve this controversy, we explored the K⁺ permeability of the IMM using whole-IMM patch-clamp electrophysiology. We identified that the IMM has a small K⁺ conductance mediated by a previously unidentified uniporter for monovalent cations (UMC). UMC is almost equally permeable to K⁺, Na⁺ and Cs⁺. Its unitary currents cannot be resolved and are compatible with either a very low-conductance channel or a transporter. UMC is inhibited by quinine derivatives, Ca²⁺ channel blockers, and sigma-2 receptor agonist. At the intact-mitochondria level, these inhibitors demonstrate that slow mitochondrial K⁺ uptake via UMC does not cause measurable mitochondrial depolarization. However, UMC emerges as crucial for regulation of mitochondrial volume, phosphate import, ATP production and respiration in general. In conclusion, the IMM contains a K⁺-permeable uniporter that paradoxically benefits oxidative phosphorylation and was an overlooked factor in the original formulation of the chemiosmotic theory.