The biogeochemical sulfur cycle plays a central role in fueling microbial metabolisms, regulating the redox state of the Earth, and impacting climate through remineralization of organic carbon. However, traditional reconstructions of the ancient sulfur cycle based on geochemistry are confounded by ambiguous isotopic signals, low sulfate concentrations in the Archean ocean, and the isotopic impacts of photolysis acting on volcanogenic SO2 gas. Here, we use a phylogenomics approach to ascertain the timing of gene duplication, loss, and horizontal gene transfer events for sulfur cycling genes across the tree of life. Our results suggest that metabolisms using sulfate reduction and sulfide oxidation emerged early in life's evolution, but metabolic pathways involving thiosulfate and the sox pathway proliferated across the tree of life only after the Great Oxidation Event, suggesting enhanced recycling of sulfur with increasing oxygen levels in the Paleoproterozoic ocean. Moreover, our results provide the first indication of organic sulfur cycling in the Archean with implications for climate regulation and atmospheric biosignatures. Overall, our results provide new insights into how the biological sulfur cycle evolved in tandem with the redox state of the early Earth and illustrate the power of combining geochemical and bioinformatics approaches to understand the evolution of Earth over time.