The solvation free energy of the peptide backbone is conformation-dependent. Abstract: Does aqueous solvent discriminate among peptide conformers? To address this question, we computed the solvation free energy of a blocked, 12-residue polyalanyl-peptide in explicit water and analyzed its solvent structure. The peptide was modeled in each of 4 conformers: ALPHA-helix, antiparallel BETA-strand, parallel BETA-strand, and polyproline II helix (PII). Monte Carlo simulations in the canonical ensemble were performed at 300 K using the CHARMM 22 force field with TIP3P water. The simulations indicate that the solvation free energy of PII is favored over that of other conformers for reasons that defy conventional explanation. Specifically, in these 4 conformers, an almost perfect correlation is found between a residue's solvent-accessible surface area and the volume of its first solvent shell, but neither quantity is correlated with the observed differences in solvation free energy. Instead, solvation free energy tracks with the interaction energy between the peptide and its first-shell water. An additional, previously unrecognized contribution involves the conformation-dependent perturbation of first-shell solvent organization. Unlike PII, BETA-strands induce formation of entropically disfavored peptide:water bridges that order vicinal water in a manner reminiscent of the hydrophobic effect. The use of explicit water allows us to capture and characterize these dynamic water bridges that form and dissolve during our simulations.