Methyl-coenzyme M reductase (MCR) catalyzes the terminal reaction in methanogenesis, the formation of methane from methyl-coenzyme M and coenzyme B. The active site of MCR binds the prosthetic group F(430), a unique nickel hydrocorphin cofactor. Here, spectroscopy and computations are employed in developing detailed electronic descriptions of the Ni(II) and Ni(I) forms of the free cofactor. Absorption, magnetic circular dichroism (MCD), and variable-temperature variable-field MCD data are analyzed within the framework of time-dependent DFT computations to assign key electronic transitions. DFT calculations are further employed to evaluate possible reduced F(430) models-a one-electron reduced Ni(I)F(430) model and a three-electron reduced Ni(I)F(red430) model (possessing a reduced hydrocorphin ligand)-on the basis of excited-state spectra and published EPR/ENDOR parameters. While calculations on both models yield spectroscopic parameters that are consistent with most experimental data, overall better agreement is achieved using the Ni(I)F(430) model, particularly with respect to electronic absorption and (1)H ENDOR. The experimentally validated bonding descriptions generated herein show that in Ni(II)F(430) the occupied Ni 3d orbitals are too low in energy to significantly perturb the dominant electronic transition involving the pi and pi* frontier MOs of the macrocycle (i.e., the HOMO-->LUMO transition). Upon one-electron reduction of the Ni(II) ion, the occupied Ni 3d orbitals are raised in energy, shifting between the HOMO and the LUMO of the oxidized cofactor. These ground-state changes have a dramatic effect on the excited-state structure, causing a blue shift of the dominant pi-->pi* transition and the appearance of numerous Ni 3d-->hydrocorphin pi* charge-transfer features in the vis/near-IR region.