Acinetobacter baumannii is a Gram-negative human pathogen associated with significant morbidity and mortality. The WHO has placed A. baumannii as the top critical pathogen in need for novel antimicrobial therapies due to the emergence of carbapenems resistant isolates. Metal ions, such as zinc, have been recognised as important antimicrobials to control bacterial infections. Thus, resistance to metal intoxication is crucial for the success of many pathogenic bacteria. A. baumannii is known to harbour an extensive repertoire of metal ion efflux systems, none of which have been functionally characterised. Here, we investigated the role of membrane transport systems in A. baumannii zinc resistance. Our analyses of transposon mutant A. baumannii strains revealed a role for the resistance nodulation division (RND) transporter CzcCBA in zinc resistance. This was determined by supplementing the mutant strain czcA::T26 with zinc, and examining the impact on growth and metal accumulation compared to the wild-type strain. The significance of this pathway was then investigated using a zinc-deficient murine infection model. This revealed that A. baumannii resistance to zinc stress was important in the spleen, as indicated by the reduced bacterial burden of the czcA::T26 strain by comparison to the wild-type strain. Our studies also identified an additional zinc resistance pathway, the cation diffusion facilitator (CDF) protein CzcD. We then investigated the contribution of these pathways in resistance of other transition metal ions. This revealed that CzcCBA contributed to cadmium resistance, and while CzcD did not provide resistance against cadmium, we identified a distinct CDF transporter, CzcE, that is crucial for A. baumannii survival in cadmium stress. Collectively, these analyses provide novel insights into the metal ion resistance mechanisms of A. baumannii, and the niches in which metal ion tolerance are important during infection.