Acinetobacter baumannii is a Gram-negative human pathogen associated with significant morbidity and mortality. This is attributed to the bacterium’s ubiquitous nature, high level of antibiotic resistance and expression of a broad arsenal of antimicrobial stress resistance mechanisms. A. baumannii is known to harbour an extensive repertoire of metal ion efflux systems, but none of these have been functionally characterised. Here, we study the role of membrane transport systems in A. baumannii zinc and cadmium resistance. Our analyses of mutant derivatives revealed a primary role for the CzcCBA heavy metal efflux system in zinc resistance. In addition to CzcCBA, CzcD, a member of the cation diffusion facilitator (CDF) superfamily, and CzcI, a putative periplasmic zinc chaperone, aid in A. baumannii zinc resistance. Although genetically clustered, in depth analyses reveal that czcI, czcCBA and czcD have distinct regulatory elements, with czcCBA also holding a role in resistance to the heavy metal cadmium. Further analyses of CDF members identified czcE as the primary A. baumannii cadmium efflux system. Overall, we provide novel insight into the metal ion resistance mechanisms of A. baumannii and the role these systems play in enabling the bacterium to survive in diverse environments and cause significant human disease. As CDFs span multiple domains of life, these findings are of major significance across metal ion biology.