SUMMARYSpider dragline silk has enormous potential for the development of biomimetic fibers that combine strength and elasticity in low density polymers. These applications necessitate understanding how silk reacts to different environmental conditions. For instance, spider dragline silk 'supercontracts' in high humidity. During supercontraction, unrestrained dragline silk contracts up to 50% of its original length and restrained fibers generate substantial stress. Here we characterize the response of dragline silk to changes in humidity before, during and after supercontraction. Our findings demonstrate that dragline silk exhibits two qualitatively different responses to humidity. First, silk undergoes a previously unknown cyclic relaxation-contraction response to wetting and drying. The direction and magnitude of this cyclic response is identical both before and after supercontraction. By contrast, supercontraction is a 'permanent' tensioning of restrained silk in response to high humidity. Here, water induces stress, rather than relaxation and the uptake of water molecules results in a permanent change in molecular composition of the silk, as demonstrated by thermogravimetric analysis (TGA). Even after drying, silk mass increased by ~1% after supercontraction. By contrast, the cyclic response to humidity involves a reversible uptake of water. Dried, post-supercontraction silk also differs mechanically from virgin silk. Post-supercontraction silk exhibits reduced stiffness and stress at yield, as well as changes in dynamic energy storage and dissipation. In addition to advancing understanding supercontraction, our findings open up new applications for synthetic silk analogs. For example, dragline silk emerges as a model for a biomimetic muscle, the contraction of which is precisely controlled by humidity alone.