Reactive Fe3+ minerals can influence methane (CH4) emissions by inhibiting microbial methanogenesis or by stimulating anaerobic CH4 oxidation. The balance between Fe3+ reduction, methanogenesis, and methane oxidation in the ferruginous Archean oceans would have controlled CH4 fluxes to the atmosphere, thereby regulating the capacity for CH4 to warm the early Earth under the Faint Young Sun. We studied CH4 and Fe cycling in anoxic incubations of ferruginous sediment from the Archean ocean analogue Lake Matano, Indonesia over three successive transfers (500 days total). Iron reduction, methanogenesis, methane oxidation, and microbial taxonomy were monitored in treatments amended with 10 mM ferrihydrite or goethite. After three dilutions, Fe3+ reduction persisted only in bottles with ferrihydrite. Enhanced CH4 production was observed in the presence of goethite. Methane oxidation was observed throughout incubations, although stoichiometry suggested that Fe3+ was not the sole electron acceptor. 16S rRNA profiles continuously changed over the course of enrichment, with ultimate dominance of unclassified members of the order Desulfuromonadales in all treatments and Rhodocyclaceae in treatments amended with CH4. Microbial diversity decreased markedly over the course of incubation, with subtle differences being observed between ferrihydrite and goethite. These results suggest that Fe3+-oxide mineralogy and availability of electron donors could have led to spatial separation of Fe3+-reducing and methanogenic microbial communities in ancient ferruginous marine sediments, potentially explaining the persistence of CH4 as a greenhouse gas throughout the Archean.