The elemental composition of proteins influences the quantities of different elements required by organisms. Here, we considered variation in the sulphur content of whole proteomes among 19 Archaea, 122 Eubacteria and 10 eukaryotes whose genomes have been fully sequenced. We found that different species vary greatly in the sulphur content of their proteins, and that average sulphur content of proteomes and genome base composition are related. Forces contributing to variation in proteomic sulphur content appear to operate quite uniformly across the proteins of different species. In particular, the sulphur content of orthologous proteins was frequently correlated with mean proteomic sulphur contents. Among prokaryotes, proteomic sulphur content tended to be greater in anaerobes, relative to non-anaerobes. Thermophiles tended to have lower proteomic sulphur content than non-thermophiles, consistent with the thermolability of cysteine and methionine residues. This work suggests that persistent environmental growth conditions can influence the evolution of elemental composition of whole proteomes in a manner that may have important implications for the amount of sulphur used by living organisms to build proteins. It extends previous studies that demonstrated links between transient changes in environmental conditions and the elemental composition of subsets of proteins expressed under these conditions.