Intrinsically disordered proteins are renowned for their structural plasticity when they undergo coupled folding and binding to partner proteins. The nuclear coactivator binding domain of CBP is a remarkable example of this adaptability as it folds into two different conformations depending on the binding partner. To understand the role of the conformational ensemble for plasticity in ligand recognition, we investigated the millisecond dynamics of this domain using relaxation dispersion NMR spectroscopy. All NMR signals originating from the domain are broadened, demonstrating that the whole domain experience conformational exchange. The dispersion data can be described by a global two-state exchange process between a ground state and an excited state populated to 8%. The three helices are still folded in the excited state but have a different packing from the ground state; the contact between helices 2 and 3 found in the ground state is broken in the excited state, and a new one is formed between helices 1 and 3. This suggests that while NCBD in the ground state has a structure similar to the complex with the ligand ACTR, the conformation of NCBD in the excited state has some similarity with that of NCBD in complex with the ligand IRF-3. The energy landscape of this domain is thus proposed to resemble the fold-switching proteins that have two coexisting native states, which may serve as a starting point for binding via conformational selection.