Hydrogen (H2) serves as a key point of interface between the geosphere and the biosphere and has likely done so since early in the history of Earth. Indeed, many of the most well accepted origin of life scenarios involve autotrophic microbial metabolisms that are fueled by redox reactions involving H2, including the processes of acetogenesis and methanogenesis. Acetogens and methanogens use the iron sulfur (Fe-S) protein ferredoxin (Fd) to facilitate key electron transfers between H2 and carbon reduction. However, the redox potential of H2 (E0 = -420 mV) is not of sufficiently negative potential to drive reduction of Fd (E0 = -500 mV). Here we will examine mechanisms that allow for the reduction of Fd with H2 in primitive cells, with a focus on the process of electron bifurcation (EB). EB involves the simultaneous reduction or oxidation of two electron acceptors in an enzyme complex, whereby a thermodynamically favorable exergonic reaction drives a thermodynamically unfavorable endergonic reaction. Along with substrate level and oxidative phosphorylation, EB has been proposed as the third fundamental mechanism by which energy can be conserved in biological systems. Phylogenetic analyses, combined with taxonomic distribution data, are used to evaluate the ancestry of EB enzyme complexes and their role in life’s earliest metabolisms. Environmental conditions that putatively supported the earliest evolving organisms and their EB complexes are proposed. Finally, we briefly examine novel pathways that acetogens and methanogens may have used to acquire iron and sulfur to meet Fe-S biosynthetic demands in these environments.