The proton NMR spectra of unlabeled alanine dipeptide (Ac-L-Ala-NHMe) at 300 MHz and of alanine dipeptide with a single C-13 label at 500 MHz are obtained in the lyotropic liquid-crystalline solvent cesium pentadecafluorooctanoate in water (CsPFO/H2O). Simulations of the spectra yield 9 and 13 dipolar couplings D-ij, respectively, many with absolute sign determined. We fit the set of dipolar couplings by systematically varying the flexible dihedral angles phi and psi while freezing local geometric details from the electronic structure calculations of Suhai and co-workers (Han, W. G.; Jalkanen, K. J.; Elstner, M.; Suhai, S. J. Phys. Chem. B 1998, 102, 2587). The orientation tensor is optimized at each combination of dihedral angles. Remarkably, a single conformer P-II (phi approximate to-85degrees, psi approximate to+160degrees) fits both sets of couplings within experimental error. The orientation tensor can be understood in terms of a simple rocking motion that dips the central methyl group into the fluorocarbon core of the CsPFO bicelle while alternately exposing both hydrogen-bonding pockets of P-II to interfacial or bulk water. The search for a minority conformer such as alpha(R) (right-handed alpha helix, often favored by theory) using the larger data set was inconclusive. The data support localization of the peptide within the P-II well rather than the broad sampling of 0 in the range from -60degrees to -180degrees (a "beta/P-II minimum") found by certain models. We suggest that the P-II geometry is stable primarily because it maximizes the opportunity for peptide-water cooperative hydrogen bonding, whereas the alpha(R) geometry is stable primarily because of its large dipole moment. Our result corroborates recent work on short polypeptides suggesting that they preferentially sample configurations that fluctuate about P-II-like structures, in contrast to the usual random-coil models.