The most widely accepted scientific theory for the origin of life on Earth is that prokaryotic microbes evolved from simple organic compounds in seawater under anoxic conditions. For about 1 billion years thereafter, these microbes consumed the same dissolved organic matter (DOM) from which they had evolved before scarcity of DOM forced the evolution of cyanobacterial photosynthesis followed by eukaryosis. Could the more efficient consumption of DOM have also stimulated the subsequent origin of multicellular animal life? In this report, we synthesize past and recent evidence to propose the “DOM uptake hypothesis” for the origin of metazoans. A choanoflagellate-like protozoan was the likely ancestor of the first sponge-like metazoan to evolve on Earth. Choanoflagellates have outwardly facing flagellae that are subject to viscous water movement, while sponges have choanocytes in chambers with flagellae directed to pump water with greater fluidity across an aquiferous system with a huge cellular surface area. While generally considered particle feeders, both choanoflagellates and sponges absorb DOM, with some sponges relying on DOM for as much as 90% of their diet. We propose that the earliest metazoans may have evolved to survive the dire nutritional conditions of the Cryogenian “snow-ball Earth” period (~700 million years ago) by developing a body plan with the enhanced ability to absorb low concentrations of DOM in seawater from sources such as the viral lysis of microbes, exudates of benthic stromatolites, or refractory DOM compounds. Additionally, species of extant sponges that have a high abundance of microbes living in their bodies consume the greatest amounts of DOM, suggesting that the DOM uptake hypothesis may also be dependent on microbial symbiosis.