Phosphorylation is one the most important reactions in life. It is a key requirement for the realisation of many of Life's essential features such as compartmentalisation (phospholipids), preservation of genetic information (DNA's phosphodiester backbone) and the prime energy transfer process to drive endergonic reactions (nucleotide triphosphates e.g. ATP). The incorporation of phosphate chemistry into prebiotic systems is thus seen as an essential requirement for the emergence of life. Here, we demonstrate the construction of a prebiotically plausible phosphate transfer system which combines formation of a KSTA ATP analogue with histidyl peptide organocatalysts (Figure ). We show first that histidyl peptides catalyse the phosphate transfer of imidazole phosphate to water (hydrolysis) via the formation of a phosphorylated histidyl intermediate and quantify rate constants for this reaction. We then demonstrate that in a paste histidyl peptides catalyse the phosphate transfer from imidazole phosphate to organic molecules via the phosphorylated histidyl intermediate. We explore how the amino acid sequence in the histidyl peptide catalyst affects its catalytic activity. Finally, we demonstrate a full physicochemical orthophosphate cycle in the presence of histidyl peptide catalysts which incorporates both the in situ formation of the KSTA imidazole phosphate and histidyl peptide catalysed phosphorylations.