The active sites of Fe-only hydrogenases (FeHases) feature an unusual polynuclear iron-sulfur cluster, known as the H-cluster, that consists of a [Fe4S4] cubane linked to a di-iron subunit (the [2Fe](H) component) via a bridging cysteine ligand (S-Cys). While previous computational studies of FeHases employed H-cluster models that only included the [2Fe]H component, we have utilized density functional theory (DFT), in conjunction with the broken-symmetry (BS) approach, to explore the geometric, electronic, and magnetic properties of the entire H-cluster. These calculations have allowed us to evaluate, for the first time, the influence of the [Fe4S4] cubane on the [2Fe](H) component of the H-cluster in its active (H-ox) and CO-inhibited (H-ox-CO) states, both of which are paramagnetic (S = 1/2). Our results reveal that the presence of the cubane tunes both the position and the donor strength of the S-Cys ligand, which, in turn, modulates the internal geometric and electronic structures of the [2Fe](H) subduster. Importantly, the BS methodology provides an accurate description of the exchange interactions within the H-cluster, permitting insight into the electronic origin of the changes in magnetic properties observed experimentally upon conversion of H-ox to H-ox-CO. Specifically, while the unpaired spin density in the H-ox state is localized on the distal Fe center, in the H-ox-CO state, it is delocalized over the [2Fe](H) component, such that the proximal Fe center acquires significant spin density (where distal and proximal refer to the positions of the Fe centers relative to the cubane). To validate our H-cluster models on the basis of experimental data, two DFT-based approaches and the semiempirical INDO/S method have been employed to compute electron paramagnetic resonance parameters for the H-cluster states. While most computations yield reasonably accurate g values and ligand hyperfine coupling constants (i.e., A values) for the H-ox and H-ox-CO states, they fail to reproduce the isotropic Fe-57 A tensors found experimentally. Finally, extension of the computational methodology employed successfully for the H-ox and H-ox-CO states to the metastable H-ox "photo state, generated by irradiation of the H-ox-CO state at cryogenic temperatures, has allowed us to discriminate between proposed structural models for this species.