Nonlocal density functional theory calculations, with full geometry optimization, are reported for the Ni(I) and low-spin Ni(II) forms of high-fidelity models of coenzyme F430, the nickel tetracorphinoid cofactor of methylcoenzyme M reductase (MCR), and its 12,13-diepimer. The diepimer appears to exhibit the conformational characteristics of a typical hydroporphyrin in terms of a strong tendency to adopt highly ruffled conformations and short Ni(II)−N bond distances. In contrast, for native F430, the steric effects of peripheral substituents impose a potent planarizing influence on the ring system. The relative inability to ruffle implies that the N4 core of F430 cannot contract sufficiently to optimally coordinate a small low-spin Ni(II) ion. This appears to be the key factor that results in the stabilization of the larger Ni(I) and high-spin Ni(II) ions by the F430 ligand environment. The optimized Ni−N bond distances for the Ni(I)−F430 model compound are 198, 200, 203, and 214 pm and span an extremely wide range of 16 pm, which qualitatively reproduces the central feature of the experimental EXAFS results. Understandably, these bond distances are similar to those found in a crystallographic study of a six-coordinate Ni(II) form of MCR. The relatively long Ni−N distances in the optimized geometry of the low-spin Ni(II) form of the F430 model compound provide a natural explanation for the enhanced axial ligand affinity of F430 and its greater tendency to switch to the high-spin Ni(II) form, relative to its diepimer. Consistent with experiment, the calculations also predict that Ni(II)−diepi-F430 is thermodynamically more stable than native Ni(II)−F430. However, for the Ni(I) oxidation level, the two epimers are predicted to be equienergetic. In qualitative agreement with electrochemical measurements, the adiabatic ionization potential of Ni(I)−F430 is about 0.2 eV higher than that of Ni(I)−diepi-F430, again reflecting a unique destabilization of low-spin Ni(II) by the F430 ligand. Finally, the nickel center in Ni(I)−F430 is truly Ni(I): it carries approximately 82% of the molecular unpaired spin, compared to a nickel spin population of only 56% for Ni(I)−diepi-F430.