Many venom peptides are potent and selective inhibitors of voltage-gated ion channels, including channels that are validated therapeutic targets for treatment of a wide range of human diseases. However, the development of novel venom-peptide-based therapeutics requires an understanding of their mechanism of action. In the case of voltage-gated ion channels, venom peptides act either as pore blockers that plug the extracellular face of the channel pore or gating modifiers that bind to one or more of the membrane-embedded voltage sensor domains. It has been debated whether membrane partitioning is an intrinsic feature of gating modifier toxins. In this study we used surface plasmon resonance and molecular dynamics to directly compare the lipid binding properties of two gating modifiers (μ-TRTX-Hd1a and ProTx-I) and two pore-blockers (ShK and KIIIA). Of the peptides tested only ProTx-I showed concentration-dependent binding to phospholipid model membranes. Our results provide further evidence that the ability to insert into the lipid bilayer is not a requirement to be a gating modifier. In addition, we have characterised the lipid interaction surface of ProTx1 to neutral and anionic phospholipid membranes.