Interproton NMR dipolar cross-relaxation rates have been calculated from a 1-ns molecular dynamics simulation of a cyclic hexapeptide, pressinoic acid, in aqueous solution. The latter shows a wide distribution of order parameters and internal correlation times, reflecting the flexibility of the system. In particular, the relative mobility of the aromatic side chains agrees with experiment. Dihedral angle dynamics are identified as a cause of correlation between the otherwise separate effects of angular and radial averaging of the interproton vector. Although internal motion is seen to be dominated by angular effects, the high sigma(dyn)/sigma(rig) ratios of several proton pairs are due to large distance fluctuations. The latter, which may occur surprisingly often in small peptides, will make rates predicted from the mean conformation appear too small. The choice of the reference proton pair used to calibrate the cross-relaxation rates for interproton distance determination is shown to significantly affect the latter.