Here we have demonstrated a plausible prebiotic precursor to Life's phosphate transfer system (Figure ). Our system is constructed by combining a kinetically stable and thermodynamically activated ATP analogue, i.e. imidazole phosphate, and a kinase enzyme analogue i.e. organocatalytic histidyl peptides. First, we showed that histidyl peptides catalyse the transfer of phosphate from imidazole phosphate with a set of hydrolysis reactions. This reaction proceeded via the formation of a phosphorylated imidazolyl histidyl -a less stable amidophosphate than imidazole phosphate. When we quantified the rate constants for this reaction we determined that histidyl peptides increase the hydrolysis rate constant by two orders of magnitude. Next, we demonstrated that upon moving to a physical environment with a lower water activity by drying to a paste, the histidyl peptides catalyse the phosphorylation of the organic nucleophile glycerol. Peptides with an N-terminal histidyl residue were observed to be the best catalysts. Finally, we integrated the histidyl peptide catalysed phosphorylations into a complete prebiotic scenario for producing phosphorylated organic compounds. Here, orthophosphate was first activated and then kinetically trapped in the form of imidazole phosphate. Upon drying to a paste, histidyl peptides catalysed the phosphorylation of both glycerol and glycerate. Repeated cycling led to a stepwise increase in the yield of phosphorylated organic compounds. This system demonstrates a plausible prebiotic route for the catalysed production of phosphorylated compounds on the early Earth.