Copper (Cu) and iron (Fe) are essential micronutrients that are toxic when accumulating in excess in cells. Thus, their uptake by roots is tightly regulated. While plants sense and respond to local Cu availability, the systemic regulation of Cu uptake has not been documented in contrast to local and systemic control of Fe uptake. Fe abundance in the phloem has been suggested to act systemically, regulating the expression of Fe uptake genes in roots. Consistently, shoot-to-root Fe signaling is disrupted in Arabidopsis thaliana mutants lacking the phloem companion cell-localized Fe transporter, OLIGOPEPTIDE TRANSPORTER 3 (AtOPT3). We report that AtOPT3 also transports Cu in heterologous systems and contributes to its delivery from sources to sinks in planta. The opt3 mutant contained less Cu in the phloem, was sensitive to Cu deficiency and mounted a transcriptional Cu deficiency response in roots and young leaves. Feeding the opt3 mutant and Cu- or Fe-deficient wild-type seedlings with Cu or Fe via the phloem in leaves downregulated the expression of both Cu and Fe-deficiency marker genes in roots. These data suggest the existence of shoot-to-root Cu signaling, highlight the complexity of Cu/Fe interactions, and the role of AtOPT3 in fine-tuning root transcriptional responses to the plant Cu and Fe needs.