The amidohydrolase superfamily (AHS) is one of the most well-characterised protein families, with over 20, 000 enzymes defined by conserved metal binding motifs and a (β/α)-barrel fold.^[1] The AHS is currently divided into eight subtypes dependent on the specific metal binding ligands that constitute the mononuclear or binuclear divalent metal centre. Molinate hydrolase (MolA), one of three founding enzymes in subtype 8 has been structurally characterised for the first time, providing insight into its function and the evolution of the AHS as a whole. Crystal data of the apo-enzyme in combination with kinetic analysis of key active site mutants has revealed a likely mononuclear metal binding site and a potential reaction mechanism for MolA with molinate. Kinetic analyses have quantified promiscuous activity distinct from the most prominent activity of MolA with the thioester pesticide molinate. These data provide a basis for understanding the evolution of MolA, enabling both future work elucidating the evolutionary pathway of the AHS and the development of MolA for use in bioremediation of molinate-contaminated areas.