Tropomyosins (TMs) are highly conserved, coiled-coil, actin binding regulatory proteins found in most eukaryotic cells. The amino-terminal domain of 284-residue TMs is among the most conserved and functionally important regions. The first nine residues are proposed to bind to the carboxyl-terminal nine residues to form the “overlap” region between successive TMs, which bind along the actin filament. Here, the structure of the N-terminus of muscle α-TM, in a chimeric peptide, TMZip, has been solved using circular dichroism (CD) and two-dimensional proton nuclear magnetic resonance (2D ¹H NMR) spectroscopy. Residues 1−14 of TMZip are the first 14 N-terminal residues of rabbit striated α-TM, and residues 15−32 of TMZip are the last 18 C-terminal residues of the yeast GCN4 transcription factor. CD measurements show that TMZip forms a two-stranded coiled-coil α-helix with an enthalpy of folding of −34 ± 2 kcal/mol. In 2D¹H NMR studies at 15 °C, pH 6.4, the peptide exhibits 123 sequential and medium range intrachain NOE cross peaks per chain, characteristic of α-helices extending from residue 1 to residue 29, together with 85 long-range NOE cross peaks arising from interchain interactions. The three-dimensional structure of TMZip has been determined using these data plus an additional 509 intrachain constraints per chain. The coiled-coil domain extends to the N-terminus. Amide hydrogen exchange studies, however, suggest that the TM region is less stable than the GCN4 region. The work reported here is the first atomic-resolution structure of any region of TM and it allows insight into the mechanism of the function of the highly conserved N-terminal domain.