Meeting global food needs in the face of climate change and resource limitation requires innovative approaches to food production. Here, we explore incorporation of new dark food chains into human food systems, drawing inspiration from natural ecosystems, the history of single cell protein, and opportunities for new food production through wastewater treatment, microbial protein production, and aquaculture. The envisioned dark food chains rely upon chemoautotrophy in lieu of photosynthesis, with primary production based upon assimilation of CH4 and CO2 by methane- and hydrogen-oxidizing bacteria. The stoichiometry, kinetics, and thermodynamics of these bacteria are evaluated, and opportunities for recycling of carbon, nitrogen, and water are explored. Because these processes do not require light delivery, high volumetric productivities are possible; because they are exothermic, heat is available for downstream protein processing; because the feedstock gases are cheap, existing pipeline infrastructure could facilitate low-cost energy-efficient delivery in urban environments. Potential life-cycle benefits include: a protein alternative to fishmeal; partial decoupling of animal feed from human food; climate change mitigation due to decreased land use for agriculture; efficient local cycling of carbon and nutrients that offsets the need for energy-intensive fertilizers; and production of high value products, such as the prebiotic polyhydroxybutyrate.