We identified vibrational spectral marker bands that sensitively report on the side chain structures of glutamine (Gln) and asparagine (Asn). Density functional theory (DFT) calculations indicate that the Amide IIIP (AmIIIP) vibrations of Gin and Asn depend cosinusoidally on their side chain OCCC dihedral angles (the chi(3) and chi(2) angles of Gin and Asn, respectively). We use UV resonance Raman (UVRR) and visible Raman spectroscopy to experimentally correlate the AmIIIP Raman band frequency to the primary amide OCCC dihedral angle. The AmIIIP structural sensitivity derives from the Gln (Asn) C-beta-C-gamma (C-alpha-C-beta) stretching component of the vibration. The C-beta-C-gamma (C-alpha-C-beta) bond length inversely correlates with the AmIIIP band frequency. As the C-beta-C-gamma (C-alpha-C-beta) bond length decreases, its stretching force constant increases, which results in an upshift in the AmIIIP frequency. The C-beta-C-gamma (C-alpha-C-beta) bond length dependence on the chi(3) (chi(2)) dihedral angle results from hyperconjugation between the C-delta=O-epsilon (C-gamma=O-delta) pi* and C-beta-C-gamma (C-alpha-C-beta) sigma orbitals. Using a Protein Data Bank library, we show that the chi(3) and chi(2) dihedral angles of Gln and Asn depend on the peptide backbone Ramachandran angles. We demonstrate that the inhomogeneously broadened AmIIIP band line shapes can be used to calculate the chi(3) and chi(2) angle distributions of peptides. The spectral correlations determined in this study enable important new insights into protein structure in solution, and in Gln- and Asn-rich amyloid-like fibrils and prions.