Characterization of the unfolded state is a fundamental prerequisite for understanding protein stability and folding. We have investigated local conformational sampling in urea-denatured ubiquitin at pH 2.5 by measuring an extensive set of residual dipolar couplings (RDCs) under conditions of partial molecular alignment. Seven experimental RDCs per peptide unit, including complementary fixed-geometry and interproton (H-1(N)-H-1(N) and H-1(N)-H-1(alpha)) couplings, were used to investigate the structural properties of the peptide chain. Amino-acid-specific potentials that simultaneously reproduce all RDCs in the molecule are found to sample more extended conformations than the standard statistical coil description. Analysis of (3)J(HNH alpha) scalar couplings measured under the same conditions suggests that neither polyproline II nor extended beta-regions dominate this additional sampling of extended conformations. Using this approach we propose a model of the conformational landscape throughout the peptide chain of urea-denatured ubiquitin, providing an essential description for understanding the unfolded state.