Abstract Photoreceptors convert the energy of light into an electric signal to be processed by the visual system. Photoreceptors of nocturnal insects are adapted for night vision by sacrificing spatial and temporal resolution for improved sensitivity. While the sensitivity-increasing optical adaptations and the temporal properties of light responses have been studied earlier, the intermediate biophysical mechanisms responsible for shaping the captured light into voltage responses were previously not known in detail in any nocturnal species. Using electrophysiological tools and computer simulations the photoreceptors of the nocturnal cockroach (Periplaneta americana) were studied by characterising 1) the electrical properties responsible for shaping the light responses, 2) the properties of light responses at different stages of light and dark adaptation and 3) properties of low-intensity light stimuli and how they are processed by the photoreceptors. The high input resistance and whole-cell capacitance were typical for a nocturnal insect, but the two voltage-dependent potassium conductances were closer to those found in diurnal species. The dominant sustained conductance typically associated with day-light vision activated during simulated light responses whereas the lesser transient conductance previously linked to low-light vision did not. Light responses were persistently slow regardless of the adapting light level and saturated at low intensities, indicating a strong adaptation to vision in dim light. Simulations showed that at such low light levels the physical noise caused by random photons determines the information rate and the biological noise, caused by random latency and amplitude of single photon responses, has only a minor effect. At higher intensities the latency variability degraded the information rates but the amplitude variability did not. Thus, photoreceptors of nocturnal animals can sacrifice phototransduction precision in their natural illumination without compromising their coding performance.