Molecular simulation has been used to model the detailed folding properties of peptides, yet prospective computational peptide design by such approaches remains challenging and nontrivial. To test the accuracy of simulation-based hairpin design, we characterized the folding properties of a series of so-called β-cap hairpin peptides designed to mimic a conserved hairpin of LapD, a bacterial intracellular signaling protein, both experimentally by NMR spectroscopy and computationally by implicit-solvent replica-exchange molecular dynamics using three different AMBER force fields (ff96, ff99sb-ildn, and ff99sb-ildn-NMR). A unique challenge presented by these designs is the presence of both a terminal Trp-Trp capping motif and a conserved GWxQ motif in the hairpin turn required for binding to LapG. Consistent with previous studies, we found AMBER ff96 to be the most accurate when used with the OBC GBSA implicit solvent model, despite its known bias toward β-sheet conformations when used in explicit-solvent simulations. To gain microscopic insight into the folding landscape of the hairpin designs, we additionally performed parallel simulations on the Folding@home distributed computing platform using AMBER ff99sb-ildn-NMR with TIP3P explicit solvent. Markov state models (MSMs) built from trajectory data reveal a number of non-native interactions between Trp and other amino acid side chains, creating potential problems in achieving well-folded hairpin structures in solution.