Pseudomonas aeruginosa is a ubiquitous, opportunistic human pathogen and a leading cause of morbidity and mortality in immunocompromised individuals. Treatment of P. aeruginosa infection is becoming increasingly difficult due to its high intrinsic and acquired resistance to multiple antibiotic classes. P. aeruginosa thrives in anaerobic and microaerophilic environments, such as the mucoid enriched lung of individuals with cystic fibrosis, generating energy via the molybdenum-dependent dissimilatory nitrate reduction pathway. In bacteria, molybdenum is acquired in the oxyanion form, molybdate, via the high-affinity ATP-binding cassette transporter ModBC and the solute binding protein ModA. Here, we biochemically characterised P. aeruginosa ModA and revealed that it was not restricted to interaction with only molybdate, its physiological ligand, but could also bind the group VI oxyanions chromate, and tungstate. High-resolution structural analyses of ModA in complex with the different metals showed that each of the oxyanions bound at the same metal binding site within the protein. Chromate is an increasingly common antimicrobial surface coating. Accordingly, we investigated whether chromate exposure induced chromate intoxication in P. aeruginosa or perturbed molybdenum homeostasis. Analysis of a modA deletion strain revealed that chromate sensitivity and cellular accumulation of the metal were not affected by loss of modA. Unexpectedly, exposure of P. aeruginosa to sub-lethal chromate stress resulted in an increase in cellular molybdenum levels in the wild-type strain and, to a lesser extent, in the ∆modA strain. This indicated that chromate-induced molybdate uptake is predominantly driven by ModA. Elemental analyses of the P. aeruginosa proteome revealed that, despite the increase in cellular molybdenum, chromate arrested the native distribution of the molybdenum within the proteome. This observation was consistent with impaired nitrate reduction and indicates a novel mechanism of chromate toxicity under anaerobic conditions. Collectively, this work advances our understanding of the biophysical properties of ModA and reveals a complex relationship between chromate toxicity and molybdenum homeostasis.