Methanosarcinales are versatile methanogens, capable of regulating most types of methanogenic pathways. Despite the versatile metabolic flexibility of Methanosarcinales, no member of this order has been shown to use formate for methanogenesis. In the present study, we identified a cytosolic formate dehydrogenase (FdhAB) present in several Methanosarcinales, likely acquired by independent horizontal gene transfers after an early evolutionary loss, encouraging re-evaluation of our understanding of formate utilization in Methanosarcinales. To explore whether formate-dependent (methyl-reducing or CO₂-reducing) methanogenesis can occur in Methanosarcinales, we engineered two different strains of Methanosarcina acetivorans by functionally expressing FdhAB from Methanosarcina barkeri in M. acetivorans. In the first strain, fdhAB was integrated into the N⁵-methyl- tetrahydrosarcinapterin:coenzyme M methyltransferase (mtr) operon, making it capable of growing by reducing methanol with electrons from formate. In the second strain, fdhAB was integrated into the F₄₂₀-reducing hydrogenase (frh) operon, instead of the mtr operon, enabling its growth with formate as the only source of carbon and energy after adaptive laboratory evolution. In this strain, one CO₂ is reduced to one methane with electrons from oxidizing four formate to four CO₂, a metabolism reported only in methanogens without cytochromes. Although methanogens without cytochromes typically utilize flavin-based electron bifurcation to generate the ferredoxins needed for CO₂ activation, we hypothesize that, in our engineered strains, reduced ferredoxins are obtained via the Rhodobacter nitrogen fixation complex complex running in reverse. Our work demonstrates formate-dependent methyl-reducing and CO₂-reducing methanogenesis in M. acetivorans that is enabled by the flexible nature of the microbe working in tandem with the nurturing provided.