SummaryCell mechanics are determined by an intracellular biopolymer network, including intermediate filaments that are expressed in a cell-type-specific manner. A prominent pair of intermediate filaments are keratin and vimentin, as they are expressed by non-motile and motile cells, respectively. Therefore, the differential expression of these proteins coincides with a change in cellular mechanics and dynamic properties of the cells. This observation raises the question of how the mechanical properties already differ on the single filament level. Here, we use optical tweezers and a computational model to compare the stretching and dissipation behavior of the two filament types. We find that keratin and vimentin filaments behave in opposite ways: keratin filaments elongate but retain their stiffness, whereas vimentin filaments soften but retain their length. This finding is explained by fundamentally different ways to dissipate energy: viscous sliding of subunits within keratin filaments and non-equilibrium α helix unfolding in vimentin filaments.