Organic semiconductors are emerging as promising candidates for novel electrically self‐sufficient photovoltaic prosthetics for neurostimulation, especially for restoration of light sensitivity in degenerate retina. Considering future applications, it is essential to gain fundamental insight into the signaling mechanisms at the organic photosensor–electrolyte–neuron interface. Particularly, targeting voltage‐gated ion channels by a pure photocapacitive stimulation is a preferred therapeutic approach as it avoids redox reactions involved in Faradaic charge injection. The present study investigates whether single neuroblastoma (N2A) cells, grown on a photosensor based on a small molecular squaraine:fullerene photoactive layer blend, optionally covered with silicon dioxide, can be activated by photocapacitive stimulation. Indeed, upon pulsed illumination, a rapid transient photocurrent strongly depolarizes the membrane potential and subsequently activates fast‐responding voltage‐gated sodium channels. The dielectric top coating on the organic layer ensures sufficient capacitive charge injection efficiency while maintaining the rapid response of the device. Due to the high irradiance level required for photocapacitive stimulation, another slower, independent, and unintended, nonelectrical signaling pathway is identified. This activates voltage‐gated potassium channels, presumably by photothermal effects. The present study provides the basis for further improvements on standalone photovoltaic neurostimulating platforms based on organic photoactive layers.