F1-ATPase (F1) is an ATP-driven motor in which three torque-generating β subunits in the α3β3 stator ring sequentially undergo conformational changes upon ATP hydrolysis to rotate the central shaft γ unidirectionally. Although extensive experimental and theoretical work has been done, the structural basis of cooperative torque generation to realize the unidirectional rotation remains elusive. In this study, using high-speed atomic force microscopy, we show that the rotorless F1 still “rotates”; in the isolated α3β3 stator ring, the three β subunits cyclically propagate conformational states in the counterclockwise direction, similar to the rotary shaft rotation in F1. This result provides clear evidence that the structural basis of unidirectionality is programmed in the stator ring. The present findings also have implications for cooperative interplay between subunits in other relevant hexameric ATPases.