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In accordance with the ideas of V.I. Vernadsky, the Earth’s biosphere can exist only because of the high degree of closure of the cyclic matter transformations carried out by all living organisms by using the energy from the Sun. In the course of its evolution, the Earth’s biosphere has undergone a number of cardinal transformations, but, at least for the last 20 million years, the gas composition of the atmosphere, and primarily the concentration of carbon dioxide, has remained practically unchanged. Nevertheless, the high degree of closure of material flows in the Earth’s biosphere seems paradoxical, since closure is not an adaptive feature of an individual undergoing natural selection for traits that give an advantage here and now (the Vernadsky–Darwin paradox). The stages in the formation of the closure of the Earth’s biosphere are considered in the context of four epochs that differ in the energy available to living organisms: (1) geochemical energy; (2) solar energy; (3) energy of oxidative phosphorylation; and (4) consumption of living flesh, predation. The paper considers possible options for resolving the VD paradox using as the example models of closed ecological systems (CES) with low species diversity. The fundamental inapplicability of ecological models with rigid metabolism for the description of CES is shown. Three mechanisms for resolving the VD paradox are proposed and the conditions for their implementation are assessed: (1) a stochastic mechanism: random selection of closing organisms (decomposers) with the corresponding stoichiometric ratios; (2) changing the consumption stoichiometry by switching catabolic pathways to different types of substances (proteins, fats, carbohydrates); and (3) changing the consumption stoichiometry by choosing food, depending on the state of internal nutrient pools. The present study leads to the conclusion that the Vernadsky–Darwin paradox can be resolved in nature by combining the mechanisms that simultaneously provide both a current competitive advantage and the ability to close trophic chains with a wide variation in the composition of material flows. Full article