Previous studies had shown that the molecular conformation of the synthetic human parathyroid hormone fragment 1--34 in dilute aqueous solution contained a local non-random structure formed by the four consecutive residues--Val-21--GIn-22--Trp-23--Leu-24--. This paper gives a detailed description of this local spatial structure obtained from high resolution 1H NMR studies at 360 MHZ of several peptide analogs of the partial sequence 20--24. The most important spectral parameters were high-field shifts of the alpha and gamma protons of Val-21, the spin-spin coupling constants related to the rotamer populations of the side-chains of Val-21 and Trp-23, and pH titration shifts of the amide proton resonances. It was found that the backbone fragment 20--24 is so arranged that the side-chain of Val-21 is located next to the indole ring plane of Trp-23; evidence is presented that this non-random structure is mainly stabilized by hydrophobic interactions between the side-chains of Val-21 and Trp-23. The thermal population of the observed molecular structure at room temperature was estimated from the nuclear magnetic resonance data to be approximately 20%.