When a trolleybus travels through insulated sections of the overhead contact line, it experiences momentary power interruptions, which adversely affect the vehicle’s on-board auxiliary subassemblies. To reduce these negative effects, one can harness energy recovered via regenerative braking. A model power supply circuit diagram for structural systems of the trolleybus is proposed. Simulation tests were carried out to develop a method for analyzing power supply to trolleybus auxiliary devices and verify it in a real-life example. The results allow determination of the limit power that can be generated by the trolleybus drive system to feed auxiliary devices during interruptions in power supply from the overhead contact line. The possibility of powering the on-board auxiliary equipment of a trolleybus using energy from recuperation with a traction motor is presented.