κM-conotoxin RIIIK blocks TSha1 K⁺ channels from trout with high affinity by interacting with the ion channel pore. As opposed to many other peptides targeting K⁺ channels, κM-RIIIK does not possess a functional dyad. In this study we combine thermodynamic mutant cycle analysis and docking calculations to derive the binding mode of κM-conotoxin RIIIK to the TSha1 channel. The final model reveals a novel pharmacophore, where no positively charged side chain occludes the channel pore. Instead the positive-charged residues of the toxin form a basic ring; κM-RIIIK is anchored to the K⁺ channel via electrostatic interactions of this basic ring with the loop and pore helix residues of the channel. The channel amino acid Glu-354 is likely to be a fundamental determinant of the selectivity of κM-RIIIK for the TSha1 channel. The Cγ-OH of Hyp-15 is in contact with the carbonyls of the selectivity filter, disturbing the charge distribution pattern necessary for the coordination of K⁺ ions. This novel, experimentally based pharmacophore model proves the existence of diverse binding modes of peptidic toxins to K⁺ channels and underlines the role of intermolecular electrostatic interactions involving channel loop side chains in determining the selectivity of toxins for specific K⁺ channel types.