The dispersive optical activity of (R)-(-)-glycidyl methyl ether (R-GME) has been interrogated under ambient vapor-phase and solution-phase conditions, with quantum-chemical analyses built on density functional (B3LYP and CAM-B3LYP) and coupled-cluster (CCSD) implementations of linear-response theory exploited to interpret experimental findings. Inherent flexibility of the heavy atom skeleton leads to nine low-lying structural isomers that possess distinct chiroptical and physicochemical properties, as evinced by marked changes in the magnitude and the sign of rotatory powers observed in various media. These species are interconverted by independent motion along two large-amplitude torsional coordinates and are stabilized differentially by interaction with the surroundings, thereby reapportioning their relative contributions to the collective response evoked from a thermally equilibrated ensemble. The intrinsic behavior exhibited by isolated (vapor-phase) R-GME molecules was calculated through use of both conformer-averaging and restricted vibrational-averaging procedures, the former affording moderately good agreement with measurements of optical rotatory dispersion (ORD) and the latter providing strong evidence for sizable effects arising from vibrational degrees of freedom. A similar conformer-averaging ansatz based on the polarizable-continuum model (PCM) for implicit solvation was deployed to elucidate R-GME specific-rotation parameters acquired for six dilute solutions. This approach gave reasonable predictions for sodium D-line (589.3 nm) experiments performed in the extremes of solvent polarity represented by cyclohexane and acetonitrile but failed to reproduce the overall shape of ORD profiles and suggested more complex processes might be involved in the case of an aromatic medium.