We report on extensive molecular dynamics (MD) simulations of the tridecapeptide corresponding to residues 659-671 of the envelope glycoprotein gp41 of HIV-1, which spans the 2F5 monoclonal antibody epitope ELDKWA. Previously, X-ray crystallography, nuclear magnetic resonance, and circular dichroism experiments have yielded conflicting conformational information, but there is a growing consensus that the monomeric peptide in aqueous solution is disordered. Here, we use the latest, state-of-the-art AMBER force fields to describe the complex conformational landscape of gp41(659-671). We have analyzed the conformational ensembles of the peptide in solution both without applied restraints and under successive tensile restraints. In contrast to previous MD simulations, our results are consistent with the bulk of the experimental findings. The amount of helical population is important in aqueous solution, but this structure forms part of a flexible conformational ensemble with a rugged free energy landscape with shallow minima. Under uniaxial tension, the disordered peptide first becomes fully helical before melting into turns, loops, and 3(10)-helices. The conformational ensemble includes epitope conformations close to an NMR solution structure (PDB ID 1LCX) as well as epitope conformations close to a very different, extended crystal structure (PDB ID 1TJH).