In the reaction of the binuclear non-heme iron protein hemerythrin (Hr) with dioxygen, one electron from each Fe(II) center and the proton from the bridging hydroxide of the diferrous site (deoxyHr) are transferred to O-2? binding to a single iron center (Fe2), yielding the ore-bridged diferric site possessing a terminal hydroperoxide (oxyHr). Using the experimentally calibrated bonding descriptions of oxyHr and deoxyHr developed in the accompanying paper [Brunold, T. C.; Solomon, E. I. J. Am. Chem. Sec. 1999, 121, 8277], the process of Oz release from Hr is explored through density functional calculations that interpolate between these well-defined reference electronic structures. The relevant steps are (i) elongation of the Fe2-hydroperoxide bond driving the first one-electron transfer (ET) from the peroxide to the coordinated iron (Fe2), followed by (ii) tunneling of the hydroperoxide proton to the mu-oxo bridge coupled with the second ET, from the Oz species to the noncoordinated iron (Fel). Significantly, while (ii) is a proton-coupled ET it is not an H atom transfer as the electron transfers through the same Fe-O-Fe mixed sigma/pi superexchange pathway that produces the dominant contribution to the strong antiferromagnetic coupling in oxyHr and bent ore-bridged diferric complexes in general.