The conformationally flexible fusion peptide (FP) of HIV-1 is indispensible for viral infection of host cells, due to its ability to insert into and tightly couple with phospholipid membranes. There are conflicting reports on the membrane-associated structure of FP, and solution structure information is limited, yet such a structure is the target for a novel class of antiretroviral inhibitors. An ensemble of explicit solvent molecular dynamics simulations, initiated from a disordered HIV-1 FP (aggregate time of ∼30 μs), revealed that while the vast majority of conformations predominantly lack secondary structure, both spontaneous formation and rapid interconversion of local secondary structure elements occur, highlighting the structural plasticity of the peptide. Therefore, even at this rapid time scale, FP constitutes a diverse and flexible conformational ensemble in solution. Secondary structure clustering reveals that the most prominent ordered elements are α- and 3-10-helical subsets of membrane-bound conformations, while trace populations within 2 Å RMSD of all complete membrane-bound conformations are found to pre-exist in the solution ensemble. Since inhibitor bound conformations of FP are only rarely found, FP inhibitors could function by modulating the conformational ensemble and binding to nonfusogenic FP structures. A thermodynamic characterization of the most prominent ordered nonfusogenic structures could facilitate the future design of improved FP inhibitors.