Bacterial infection involves a constant tug-of-war between host and pathogen for the essential nutrients of life. Nevertheless, how bacteria selectively acquire the essential first-row transition metal ion manganese from the host environment remains poorly understood. Here, we investigated the manganese importing ATP-binding cassette (ABC) transporter PsaBCA of Streptococcus pneumoniae, the foremost human bacterial pathogen. By combining molecular microbiological, biochemical, biophysical and structural approaches we show that specificity is achieved not by selective binding of manganese, but by the inability of ions other than manganese to be released into the transporter. Our data show that the metal-recruiting component of the pathway, PsaA, is not restricted to binding manganese and is highly permissive for interaction with any divalent first-row transition metal ion. However, biochemical assays and single molecule FRET studies show that zinc and copper ions, which are highly abundant during infection, result in the formation of PsaA-metal complexes incapable of releasing these non-cognate metal ions. Further, these PsaA-metal complexes are incapable of stimulating ATP hydrolysis in proteoliposome-reconstituted PsaBC. In contrast, manganese can be readily released from PsaA-metal complexes, and manganese-bound PsaA stimulates ATP hydrolysis in proteoliposome-reconstituted PsaBC. Collectively, these findings provide a structural basis for how manganese ions are selectively imported by the PsaBCA importer.