Huntington's disease is a neurodegenerative disorder caused by a polyglutamine (polyQ) expansion in the N-terminal fragment of the Huntingtin (Htt) protein. Structural properties of Htt N-terminal regions and the molecular mechanism leading to protein aggregation have not been fully explained yet. We performed all-atom replica exchange molecular dynamics to investigate the structures of Htt N-terminal parts with polyQ tracts of nonpathogenic and pathogenic lengths. The monomers were composed of the headpiece (17 N-terminal residues), a polyQ tract (polyQ((17)) for native and polyQ((55)) for pathogenic sequence), and a polyP((11)) region, followed by 17 amino acids of mixed sequence. We found that corresponding regions in both fragments fold to similar secondary structures; the headpiece and polyQ stretch adopt mainly alpha-helical conformations, and polyP((11)) forms the PP II-type helix. The native N-terminal fragment is more compact and stabilized by hydrophobic interactions between the surface of polyP((11)) and the amphipathic helix of the headpiece. In the pathogenic fragment the headpiece is solvent exposed and does not interact with polyP((11)). The predicted structure of the native N-terminal fragment agrees with the X-ray structure of the Htt first exon containing polyQ((17)). The structure of the pathogenic fragment adheres to an aggregation model that is mediated by the Htt headpiece.