The quantitative and predictive understanding how intrinsically disordered proteins (IDPs) interact with engineered nanoparticles has potentially important implications for new therapeutics as well as nanotoxicology. Based on a recently developed solution 15N NMR relaxation approach, the interactions between four representative IDPs with silica nanoparticles are reported at atomic detail. Each IDP possesses distinct binding modes, which can be quantitatively explained by the local amino‐acid residue composition using a “free residue interaction model”. The model was parameterized using the binding affinities of free proteinogenic amino acids along with long‐range effects, derived by site‐specific mutagenesis, that exponentially scale with distance along the primary sequence. The model, which is accessible through a web server, can be applied to predict the residue‐specific binding affinities of a large number of IDPs. Binding of four different intrinsically disordered proteins to amorphous silica surfaces was quantitatively measured at atomic resolution by NMR and could be accurately explained by a universal free residue interaction model.