Molecular dynamics simulations of the structural distributions and the associated amide-I vibrational modes are carried out for dialanine peptide in water and carbon tetrachloride. The various manifestations in nonlinear-infrared spectroscopic experiments of the distributions of conformations of solvated dialanine are examined. The two-dimensional infrared (2D-IR) spectrum of dialanine exhibits the coupling between the amide oscillators and the correlations of the frequency fluctuations. An internally hydrogen-bonded conformation exists in CCl4 but not in H2O where two externally hydrogen-bonded forms are preferred. Simulations of solvated dialanine show how the 2D-IR spectra expose the underlying structural distributions and dynamics that are not deducible from linear-infrared spectra. In H2O the 2D-IR shows cross-peaks from large coupling in the alpha -helical conformer and an elongated higher frequency diagonal peak, reflecting the broader distribution of structures for the more flexible acetyl end. In CCl4, the computed cross-peak portion of the 2D-IR shows evidence of two amide-I transitions in the high-frequency region which are not apparent from the diagonal peak profile. The vibrational frequency inhomogeneity of the amide-I band arises from fluctuations of the instantaneous normal modes of these conformers rather than the shifts induced by hydrogen bonding. The simulation shows that there are correlations between fluctuations of the acetyl and amino end frequencies in H2O that arise from mechanical coupling and not from hydrogen bonding at the two ends of the molecule. The angular relationships between the two amide units which also show up in 2D-IR were computed, and spectral manifestations of them are discussed. The simulations also permit a calculation of the rate of energy transfer from one side of the molecule to the other. From these calculations, 2D-IR spectroscopy in conjunction with simulations is seen to be a promising tool for determining dynamics of structure changes in dipeptides.