Significance The prevailing dogma is that access to copper (Cu + ) is restricted to the extent that protein–protein interactions mediate the routing of Cu + from transporters in the plasma membrane to target cuproenzymes or transporters within subcellular compartments. The soluble proteins that distribute Cu + are called metallochaperones. Although the chloroplast requires Cu + , a chaperone that delivers this essential cofactor has remained a missing link in the model for plastid Cu + delivery. Using a comparative genomic approach and validating by biochemical characterization, we have discovered a missing chaperone. Uniquely, the previously unidentified chaperone family has evolved from the transporter to which it delivers Cu + . We also uncover an interaction between the thylakoid-localized transporter and the Cu + chaperone for stromal Cu/Zn superoxide dismutase, which highlights the complexity of Cu + distribution networks.