Relaxation dispersion NMR spectroscopy has become a valuable probe of millisecond dynamic processes in biomolecules that exchange between a ground (observable) state and one or more excited (invisible) conformers, in part because chemical shifts of the excited state(s) can be obtained that provide insight into the conformations that are sampled. Here we present a pair of experiments that provide additional structural information in the form of residual dipolar couplings of the excited state. The new experiments record H-1 spin-state selective (CO)-C-13 and C-13(alpha) dispersion profiles under conditions of partial alignment in a magnetic field from which two-bond (HN)-H-1-(CO)-C-13 and one-bond H-1(alpha)-C-13(alpha) residual dipolar couplings of the invisible conformer can be extracted. These new dipolar couplings complement orientational restraints that are provided through measurement of (HN)-H-1-N-15 residual dipolar couplings and changes in (CO)-C-13 chemical shifts upon alignment that have been measured previously for the excited-state since the interactions probed here are not collinear with those previously investigated. An application to a protein-ligand binding reaction is presented, and the accuracies of the extracted excited-state dipolar couplings are established. A combination of residual dipolar couplings and chemical shifts as measured by relaxation dispersion will facilitate a quantitative description of excited protein states.