Metallochaperones traffic copper (Cu<
sup>
+<
/sup>
) from its point of entry at the plasma membrane to its destination. In plants, one destination is the chloroplast, which houses plastocyanin, a Cu-dependent electron transfer protein involved in photosynthesis. In this paper, we present a previously unidentified Cu<
sup>
+<
/sup>
chaperone that evolved early in the plant lineage by an alternative-splicing event of the pre-mRNA encoding the chloroplast P-type ATPase in Arabidopsis 1 (PAA1). In several land plants, recent duplication events created a separate chaperone-encoding gene coincident with loss of alternative splicing. The plant-specific Cu<
sup>
+<
/sup>
chaperone delivers Cu<
sup>
+<
/sup>
with specificity for PAA1, which is flipped in the envelope relative to prototypical bacterial ATPases, compatible with a role in Cu<
sup>
+<
/sup>
import into the stroma and consistent with the canonical catalytic mechanism of these enzymes. The ubiquity of the chaperone suggests conservation of this Cu<
sup>
+<
/sup>
-delivery mechanism and provides a unique snapshot into the evolution of a Cu<
sup>
+<
/sup>
distribution pathway. Finally, we also provide evidence for an interaction between PAA2, the Cu<
sup>
+<
/sup>
-ATPase in thylakoids, and the Cu<
sup>
+<
/sup>
-chaperone for Cu/Zn superoxide dismutase (CCS), uncovering a Cu<
sup>
+<
/sup>
network that has evolved to fine-tune Cu<
sup>
+<
/sup>
distribution.