The outer membrane of Gram-negative bacteria functions as a permeability barrier to the external environment, leaving the selective uptake of nutrients to be performed by integral outer membrane proteins. These proteins are synthesized in the cytoplasm of the cell, and are delivered to their site of action by an intricate network of protein complexes, including the periplasmic chaperone, Skp. This molecule is a trimer with a "jellyfish-like" architecture, composed of a small beta-sheet "head" domain and three long alpha-helical "tentacles" encompassing a large central cavity. Whilst the tips of these tentacles come together to form an apparently closed cavity, the substrates of Skp are diverse in size, varying between 24 kDa to 85 kDa in mass, suggesting that Skp must be adaptable and/or dynamic. Based initially on X-ray crystallographic models, we reconstructed full-length trimeric Skp, and subsequently combined microsecond-timescale molecular dynamics simulation sampling with small angle X-ray scattering (SAXS) and NMR to explore its conformational landscape. The tips of Skp's tentacle-like arms were observed to spontaneously dissociate and reassemble during simulations. Based on filtering of low frequency motions, we defined hypothetical extreme closed- and open-state models, and a switching mechanism via a putative hinge region within the tentacles, consistent with dynamics measurements from NMR. Comparison of simulation structures with SAXS data confirmed that the chaperone exists in a dynamic equilibrium between open and closed states in solution. A remarkable spontaneous expansion of up to 12 nm between tentacles, previously unobserved in crystallographic studies, resolves the ability of Skp to adapt to variable cargo size in vivo.