Significance In order to understand the evolution of complex biological machines like the bacterial flagellar motor, it is crucial to know what each component does and when it arose. Here, we show that a subcomplex of the motor thought to act as a bushing for the spinning motor likely also serves another function—it plugs the hole in the outer membrane left when the flagellum disassembles. Moreover, this component and function is ancient, since it appears in diverse phyla without evidence of recent gene transfer.