The effect of the polarity of the environment on the conformation of the zwitterionic membrane lipid head groups phosphoethanolamine (PE) and phosphocholine (PC) has been investigated with calculations at the Hartree-Fock level using the 3-21G(*), 6-31G*, and 6-31+G* basis sets together with the Onsager continuum solvation model. Results suggest that in the gas phase both PE and PC adopt cyclic minimum energy conformations, in which an ammonium or N-methyl hydrogen closely approaches one of the nonesterified phosphate oxygens. In the case of PE, intramolecular interactions result in a proton transfer from the ammonium group to the phosphate oxygen, which however is suppressed by a moderate increase in the polarity of the surrounding medium. With increasing polarity of the environment, the cyclic structures of PE and PC still remain low-energy conformers but simultaneously for both head groups an almost identical extended conformer, typical of crystal structures, becomes increasingly favored. Already at epsilon = 10, the extended conformer of PC is favored (-2.4 kcal/mol) relative to the cyclic one, while for PE the relative energy of the extended conformer approaches that of the cyclic one at epsilon = 80. The similarity and increasing stability of the extended PE/PC conformers in the monomeric state and the fact that this conformer is also adopted in all crystal structures of PE/PC lipids, regardless of hydration and interaction pattern, indicate that the geometry of this conformer is determined by energetics intrinsic to the phosphoethanolammonium backbone. In lipid aggregates or a membrane environment the extended conformer becomes additionally stabilized by intermolecular ionic and hydrogen bond interactions with neighboring molecules substituting for the internal interaction that in the monomeric state constrains the zwitterionic dipole into a cyclic structure.