The human immunodeficiency virus (HIV) is "enveloped" by a membrane, and infection of a host cell begins with fusion between viral and target cell membranes. Fusion is catalyzed by the HIV gp41 protein which contains a functionally critical similar to 20-residue apolar "fusion peptide" (HFP) that associates with target cell membranes. In this study, chemically synthesized HFPs were associated with host-cell-like membranes and had "scatter-uniform" labeling (SUL), that is, only one residue of each amino acid type was U-C-13, N-15 labeled. For the first sixteen HFP residues, an unambiguous C-13 chemical shift assignment was derived from 2D C-13/C-13 correlation spectra with short mixing times, and the shifts were consistent with continuous beta-strand conformation. C-13-C-13 contacts between residues on adjacent strands were derived from correlation spectra with long mixing times and suggested close proximity of the following residues: Ala-6/Gly-10, Ala-6/Phe-1 1, and Ile-4/Gly-13. Specific antiparallel beta-strand registries were further tested using a set of HFPs that were (CO)-C-13-labeled at Ala-14 and N-15-labeled at either Val-2, Gly-3, Ile-4, or Gly-5. The solid-state NMR data were fit with 50-60% population of antiparallel HFP with either Ala14/Gly-3 or Ala-14/Ile-4 registries and 40-50% population of structures not specified by the NMR experiments. The first two registries correlated with intermolecular hydrogen bonding of 15-16 apolar N-terminal residues and this hydrogen-bonding pattern would be consistent with a predominant location of these residues in the hydrophobic membrane interior. To our knowledge, these results provide the first residue-specific structural models for membrane-associated HFP in its beta-strand conformation.