The global spread of multi-drug resistant Acinetobacter baumannii infections urgently calls for the identification of novel drug targets. We solved the cryo- electron microscopy structure of the F1Fo-ATP synthase from A. baumannii in three distinct conformational states. The nucleotide-converting F1 sub-complex reveals a specific self-inhibition mechanism, which supports a uni-directional ratchet mechanism to avoid wasteful ATP consumption. In the membrane-embedded Fo complex, the structure shows unique structural adaptations along both the entry and exit pathways of the proton-conducting a-subunit. These features, absent in mitochondrial ATP synthases, represent attractive targets for the development of next generation therapeutics that can act directly at the culmination of bioenergetics in this clinically relevant pathogen.