Flexibility in complexes between intrinsically disordered proteins and folded ligands is widespread in nature. However, timescales and spatial amplitudes of such dynamics remained unexplored for most systems. Here, we directly measure the dynamics in an exceptionally mobile, high-affinity complex. We show that the disordered tail of the cell adhesion protein E-cadherin dynamically samples a large surface area of the protooncogene β-catenin. Single-molecule experiments and molecular simulations resolve these motions with high resolution in space and time. The energy landscape of this complex is rugged with many small barriers (3 to 4 kBT). Contacts break and form within hundreds of microseconds without a dissociation of the complex. A few persistent interactions provide specificity whereas unspecific contacts boost affinity. This Velcro-like design of many weak contacts on top of a few persistent interactions reconciles three seemingly contradictory factors: specificity, high affinity, and flexibility.