The catalytically active cluster of [FeFe]‐hydrogenase (H‐cluster) is unique due to its chemical composition and electronic and geometric structures. Protein crystallography revealed the presence of biologically unique diatomic ligands coordinating to the Fe centers and three light atoms bridging the sulfur atoms of its [2Fe]‐subcluster. The identity of the light atoms remains uncertain, even at close to atomic resolution (1.39 Å), as well as due to the lack of understanding at the molecular level of the cluster's biosynthetic pathway. By using all of the proposed ligand compositions, we carried out a comprehensive electronic structure analysis by evaluating the topology of the electron density and, particularly, the atomic spin density distribution derived from various population analysis methods for the free dithiolate ligands, the biomimetic [2Fe] complexes, and the entire H‐cluster embedded in its approximately 3.5 Å protein environment. In the biomimetic model complexes we found substantial spin density delocalization at the bridgehead of the dithiolate ligands. We attributed the presence of spin density to the through‐space spin polarization interaction between the paramagnetic iron centers and the bridgehead group, as represented by the ring critical points for the [Fe–(S–R–S)–Fe] metallacycles. However, this spin polarization of the bridgehead group vanishes for some of the biomimetic models, as well as for the 208‐atom computational model of the H‐cluster, due to a network of weak interactions. When the bridgehead group becomes part of a conduit for transmitting the spin polarization towards the terminal ends of each interaction network, such as the distal water or H‐bonded residues, the spin density vanishes. The variations of the Fe atomic spin densities were compared and contrasted for the proximal and distal iron sites in the crystallographic and the rotated conformations, respectively.