In summary, we show here the development of a RaPID workflow that can select for covalent reaction between peptide and target by directly incorporating an electrophilic warhead into each member of the peptide library, whilst negatively selecting for non-covalent interactions, even if they are low nanomolar binders, like PADI4_3. We have used flexizymes to genetically encode covalency into mRNA display, specifically 2, a cysteine reactive, fluoroamidine-based warhead. Using this approach we have developed some of the most potent covalent inhibitors of PADI4 identified to date. In the future, these covalent libraries could be used to identify covalent cyclic peptide inhibitors of a range of related therapeutically relevant enzymes, including bacterial arginine deiminases, the cardiovascular target, DDAH, and the inflammatory target, STING, which has previously been shown to react with Cl-amidine. More generally, we also envisage this RaPID workflow could be applied with any other covalent warhead which can be loaded using flexizymes to target a wider range of cysteine and non-cysteine residues in therapeutic targets.