F1Fo ATP synthase interchanges phosphate transfer energy and proton motive force via a rotary catalytic mechanism and isolated F1-ATPase subcomplexes can also hydrolyze ATP to generate rotation of their central g rotor subunit. As ATP is hydrolyzed, the F1-ATPase cycles through a series of conformational states that mediates unidirectional rotation of the rotor. However, even in the absence of a rotor, the a and b subunits are still able to pass through a series of conformations, akin to those that generate rotation. We used cryo-electron microscopy to establish the structures of these rotorless states. These structures indicate that cooperativity in this system is likely mediated by contacts between the b subunit lever domains, irrespective of the presence of the g rotor subunit. These findings provide insight into how long-range information may be transferred in large biological systems.