Dimyristoylphophatidylcholine (DMPC) has been entirely or selectively deuterated on the headgroup, glycerol backbone, and acyl chains. Solid-state deuterium and phosphorus NMR was applied to this lipid with the aim to comprehensively depict its structure and dynamics when embedded in bicelles or in liposomes. Molecular mechanics calculations were also accomplished on fully hydrated DMPC bilayers. The main results are fourfold. (a) The local lipid dynamics across the entire membrane thickness could be accurately described:  the glycerol backbone shows a very restricted motional freedom and can be considered as a semirigid “rotula” separating two very fluid zones, the phosphocholine headgroup facing the water medium and the acyl chains constituting the oily bilayer interior. (b) The location of the principal axis of motion of the glycerol backbone of DMPC and its molecular order parameter, S mol, were calculated by making use of NMR, molecular mechanics, and X-ray data reported in earlier studies. Although the later lacks in accurate structural data for hydrogen atoms, there is nonetheless a general trend for an orientation of the glycerol g2−g3 carbon−carbon bond at about 28° with respect to the bilayer normal and for a S mol value of 0.55 for 78% DMPC embedded in bicelles. (c) The two DMPC conformers A and B that were earlier reported in the crystal (Pearson, H.; Parsher, I. Nature 1979, 181, 499−501) also exist in all molecular dynamics runs of fully hydrated DMPC. (d) There is a marked decrease of the DMPC phase transition temperature upon increasing selective deuterium content in the lipid structure. Interestingly, labeling of the five glycerol backbone positions induces the same temperature decrease as a full chain deuteration (54 positions).