Interactions between proteins and metal cations are central to biochemical processes and shape protein structures. SilE, an intrinsically disordered protein involved in bacterial silver-resistance, folds into α-helices upon binding Ag⁺ ions. Focusing on the B1 peptide fragment from SilE, we investigate the mechanism of Ag⁺-induced folding with simulations and NMR experiments. We first derive force-field parameters for Ag⁺-protein interactions using DFT. Then, we use replica-exchange simulations, deep learning and NMR to map B1’s folding landscape and reveal how Ag⁺ shapes it. Specifically, Ag⁺ binding promotes folding by entropic penalizing the disordered state and electrostatic stabilization of the folded state. We also describe how Ag+ alters the folding pathway. Overall, we improve the understanding of metal-induced protein folding and lay the groundwork for further computational investigations of the bacterial silver-resistance machinery.