De novo protein design is advancing rapidly. However, most designs are for single states. Here we report a de novo designed peptide that forms multiple helical-bundle states that are accessible and interconvertible under the same conditions. Usually in such designs amphipathic helices associate to form compact structures with consolidated hydrophobic cores. However, recent rational and computational designs have delivered open helical barrels with functionalisable cavities. By placing glycine judiciously in the helical interfaces of an helical barrel, we obtain both open and compact states in a single protein crystal. Molecular dynamics simulations indicate a free-energy landscape with multiple and interconverting states. Together, these findings suggest a frustrated system in which steric interactions that maintain the open barrel and the hydrophobic effect that drives complete collapse are traded-off. Indeed, addition of a hydrophobic co-solvent that can bind within the barrel effects the switch between the states both in silico and experimentally.