Because of their inherent structural plasticity, intrinsically disordered proteins (IDPs) are generally difficult to characterize, both experimentally and via simulations. In this work, an approach for studying IDPs within the potential energy landscape framework is implemented and tested. Specifically, human CD4 receptor peptide, a disordered region implicated in HIV-1 infection, is characterized via basin-hopping parallel tempering and discrete path sampling. We also investigate the effects of three state-of-the-art AMBER force fields (ff99SB-ILDN, ff14ipq, and ff14SB) on the energy landscape. The results for ff99SB-ILDN exhibit the best agreement with experiment. Metastable states identified on the free energy surface help to unify, and are consistent with, several earlier predictions, and may serve as starting points for probing the reaction interface between CD4 and HIV-1 accessory proteins.