The F1Fo ATP synthase rotary motor produces the majority of cellular energy in most cells. We have previously reported cryo-EM maps of the autoinhibited E. coli enzyme that were imaged without addition of nucleotide, which indicated that the subunit ε C-terminal domain engages with the a, b and g subunits to lock the motor and prevent functional rotation. We now present multiple cryo-EM reconstructions of the enzyme frozen in the presence of ATP to identify the conformational changes that occur when this e inhibition is removed. Although the enzyme hydrolyzes ATP, freezing soon after the addition of ATP ensures that the majority remains unconsumed. The maps generated show that, in the presence of ATP, E. coli F1Fo ATP synthase adopts a different conformation with one of the three b catalytic subunits changing its conformation substantially, from an open to a closed state. Further classification reveals multiple sub-states whereby the ε C-terminal domain transitions via an intermediate “half-up” state to a condensed “down state”. Overall this work provides direct evidence for unique conformational states that occur in E. coli ATP synthase upon ATP-induced escape from the e-inhibited state