In addition to promoting unfolded protein states, the denaturants urea and guanidinium (Gdm+) accumulate at the surface of folded proteins at subdenaturing concentrations, a phenomenon that correlates with their denaturant activities. The enhanced accumulation of Gdm+ relative to urea indicates different binding modes, or additional binding sites, for Gdm+, and we recently proposed potential binding modes to protein functional groups for Gdm+ based on the determination of the weak hydration properties of this complex cation. Here we describe molecular dynamics simulations of a model helical peptide, melittin, in a 3 M solution of GdmCl, to identify potential interactions with amino-acid side chains in a nondenatured polypeptide surface. The simulations indicate that Gdm+ can interact with a number of planar amino-acid side chains (Arg, Trp, Gln) in a stacking manner, as well as more weakly with hydrophobic surfaces composed of aliphatic side chains, and that these interactions result in enhanced number densities of Gdm+ at certain locations on the peptide surface. These observations provide molecular scale insight into the accumulation of Gdm+ at protein surfaces that has previously been observed experimentally.