Membrane-binding interfaces of peripheral proteins are restricted to a small part of their exposed surface, so the ability to engage in strong selective interactions with membrane lipids at various depths in the interface, both below and above the phosphates, is an advantage. Driven by their hydrophobicity, aromatic amino acids preferentially partition into membrane interfaces, often below the phosphates, yet enthalpically favorable interactions with the lipid headgroups, above the phosphate plane, are likely to further stabilize high interfacial positions. Using free-energy perturbation, we calculate the energetic cost of alanine substitution for 11 interfacial aromatic amino acids from 3 peripheral proteins. We show that the involvement in cation-π interactions with the headgroups (i) increases the ΔΔGtransfer as compared with insertion at the same depth without cation-π stabilization and (ii) can contribute at least as much as deeper insertion below the phosphates, highlighting the multiple roles of aromatics in peripheral membrane protein affinity.