Weak ampholytes are ubiquitous in nature and commonly found in artificial pH-responsive systems. However, our limited understanding of their ionisation response and the lack of predictive capabilities hinder the bottom-up design of such systems. Here, we used a coarse-grained model of a flexible polymer with weakly ionisable monomer units to quantitatively analyse the ionisation behaviour of two oligopeptides. Differences in ionisation response between oligopeptides and monomeric amino acids showed that electrostatic interactions between weak acid and base side chains play a key role in oligopeptide ionisation, as predicted by our model. Moreover, by comparing our simulations with experimental results from potentiometric titration, capillary zone electrophoresis and NMR, we demonstrated that our model reliably predicts the ionisation response and electrophoretic mobilities of various peptide sequences. Ultimately, our model is the first step towards using predictive bottom-up design of responsive ampholytes to tailor their properties as a function of charge and pH.