We recently reported a prebiotically plausible kinetically stable and thermodynamically activated ATP analogue in the form of imidazole phosphate. Imidazole phosphate forms under the mildest of conditions (pH 7.3, 22 °C) from a solution of cyanate, orthophosphate and imidazole. Like ATP, imidazole phosphate has good hydrolytic stability and is thus accumulated in solution. Phosphate transfer from imidazole phosphate to organic compounds does not function in solution as the activity of water is too high. However, after a wet-to-dry transition from a solution to a water-depleted paste the phosphate transfer reaction from imidazole phosphate to all the basic building blocks of life occurs. This physicochemical orthophosphate cycle could have provided a continuous supply of phosphorylated organic compounds for prebiotic chemistry upon the early Earth. We now address the challenge of combining this cycle with a prebiotic form of catalysis.