The measured NMR scalar coupling constants (J-couplings) in the XpY, (X,Y adenine (A) or cytosine (Q) RNA dinucleoside monophosphates (DMPs) were assigned to the backbone (alpha,beta,gamma,delta,epsilon,zeta) and glycosidic (chi) torsion angles in order to resolve the global structure of the DMP molecules. The experimental J-couplings were correlated with the theoretical J-couplings obtained as the dynamical averages of the Karplus equations relevant to the torsion angles. The dynamical information was captured using the molecular dynamics (MD) calculation method. The individual conformational flexibility of the four DMP molecules was thus consistently probed with the NMR J-couplings. The calculated structure and flexibility of the DMP molecules depend on the sequence considered with respect to the 5' and 3' end of the DMP molecules (5'-XpY-3'). The dynamical characteristics of the two nucleosides are not equivalent even for the ApA and CpC homologues. An enhancement of the sampling in the MD calculations was achieved using five different starting structural motives classified previously for the RNA backbone in the solid phase (Richardson et al. RNA 2008, 14, 465-481). The initial structures were selected on the basis of a database search for RNA oligonucleotides. Frequent interconversions between the conformers during the MD calculations were actually observed. The structural interpretation of the NMR spectroscopic data based on the MD simulations combined with the Karplus equations indicates that the dominant conformation of the DMP molecules in solution corresponds to the A-RNA form. For similar to 52% of the total simulation time (similar to 1000 ns), the zeta(g-)-alpha(g-)-gamma(g+) backbone topology corresponding to the canonical A-RNA form was observed, with roughly equally populated C2'-and C3'-endo sugar puckers interconverting on the nanosecond time scale. However, other noncanonical patterns were also found and thus indicate their relatively high potential to be populated in the dynamical regime. For similar to 72% of the time portion when the A-RNA of the zeta-alpha-gamma combination occurred, the nucleobases were classified as being mutually stacked. The geometries of the nucleobases classified in this work as stacked were significantly more populated for the DMP molecules with adenosine at the 3' end (ApA and CpA DMPs) than the ApC or CpC RNA molecules with C at the 3' end.