To evaluate the importance of the electronic structure of CUA to its electron-transfer (ET) function, a quantitative description of the ground-state wave function of the mixed-valence (MV) binuclear Cu-A center engineered into Pseudomonas aeruginosa azurin has been developed, using a combination of S K-edge and Cu L-edge X-ray absorption spectroscopies (XAS). Parallel descriptions have been developed for a binuclear thiolate-bridged MV reference model complex ([((LCu)-Cu-iPrdacoS)(2)](+)) and a homovalent (II,II) analogue ([(LCu)-Cu-iPr2tacnS)(2)](2+), where L-iPrdacoS and L-iPr2tacnS are macrocyclic ligands with attached thiolates that bridge the Cu ions. Previous studies have qualitatively defined the ground-stare wave function of Cu-A in terms of ligand field effects on the orbital orientation and the presence of a metal-metal bond. The studies presented here provide further evidence for a direct Cu-Cu interaction and, importantly, experimentally quantify the covalency of the ground-state wave function. The experimental results are further supported by DFT calculations. The nature of the ground-state wave function of Cu-A is compared to that of the well-defined blue copper site in plastocyanin. and the importance of this wave function to the lower reorganization energy and ET function of Cu-A is discussed. This wave function incorporates anisotropic covalency into the intra- and intermolecular ET pathways in cytochrome c oxidase. Thus, the high covalency of the Cys-Cu bond allows a path through this ligand to become competitive with a shorter His path in the intramolecular ET from Cu-A to heme a and is particularly important for activating the intermolecular ET path from heme c to CUA.