The mechanisms of nonradiative deactivation of a phenylalanine residue after near-UV photoexcitation have been investigated in an isolated peptide chain model (N-acetylphenylalaninylamide, NAPA) both experimentally and theoretically. Lifetime measurements at the origin of the first pi pi* state of jet-cooled NAPA molecules have shown that (i) among the three most stable conformers of the molecule, the folded conformer NAPA B is similar to 50-times shorter lived than the extended major conformer NAPA A and (ii) this lifetime is virtually insensitive to deuteration at the NH2 and NH sites. Concurrent time-dependent density functional theory (TDDFT) based nonadiabatic dynamics simulations in the full dimensionality, carried out for the NAPA B conformer, provided direct insights on novel classes of ultrafast deactivation mechanisms, proceeding through several conical intersections and leading in fine to the ground state. These mechanisms are found to be triggered either (i) by a stretch of the NpheH bond, which leads to an H-transfer to the ring, or (ii) by specific backbone amide distortions. The potential energy surfaces of the NAPA conformers along these critical pathways have been characterized more accurately using the coupled cluster doubles (CC2) method and shown to exhibit barriers that can be overcome with moderate excess energies. These results analyzed in the light of the experimental findings enabled us to assign the short lifetime of NAPA B conformer to a number of easily accessible exit channels from the initial pi pi* surface, most importantly the one involving a transfer of electronic excitation to an n pi* surface, induced by distortions of the backbone peptide bond.