Here we report the direct incorporation of the cysteine reactive electrophile, fluoroamidine, into cyclic peptide RaPID libraries produced by in vitro translation. We apply our covalent RaPID library in a screen against PADI4 to select exclusively for peptides which are covalently bound to the target protein. Our approach yielded peptides which covalently bind to PADI4 at Cys645 and inhibit PADI4 citrullination activity, three of which have kinact/KI in the order of 10 6 M -1 min -1 . Our current method uses a cysteine reactive warhead, but it is a generally applicable strategy where any weakly reactive covalent warhead can conceivably be incorporated.