We report a molecular strategy for precise, reversible, and noninvasive photoregulation of ion-selective membrane transport. Embedding azobenzene-containing photolipids into bilayers enables nanoscale control over the interaction and mobility of small-molecule ion carriers. Photoisomerization alone produces only minor changes in baseline conductance, consistent with the limited influence of small bilayer thickness variations on ion permeability, yet it elicits striking responses in the presence of mobile carriers. A newly designed protonophore exhibits proton-selective currents that increase by up to 200-fold under UV illumination and revert to baseline within milliseconds upon blue light. These effects cannot be explained by thickness or fluidity changes. Instead, they arise from light-dependent interactions between azobenzene moieties and the carrier that increase the membrane-bound carrier concentration and lower the effective barrier for transbilayer permeation via interfacial dipole and packing modulation. Because this mechanism relies entirely on chemical design – without genetic modification – and is compatible with photoswitches operating at longer wavelengths, it establishes a versatile framework for dynamic, light-driven control of ion transport in biological membranes and synthetic nanosystems.