Recent advances in single-molecule force spectroscopy have led to better understanding of the role of mechanical force in many biological processes. Using Atomic Force Microscopy (AFM), it is possible to manipulate bio-molecules directly at a molecular level and to study their behavior under wide ranges of forces. However, from a dynamical viewpoint, it is unclear how loading force affects internal diffusion of a protein along the pulling coordinate. We propose that frictional effects between the solvent and tethered proteins extending and relaxing under a changing load considerably slow down their rate of conformational changes and subsequently their elastic response. Here we study the elastic dynamics of tethered proteins using a fast force spectrometer with sub-millisecond time resolution, combined with Brownian and Molecular Dynamics simulations. We show that the act of tethering a polypeptide to an object, an inseparable part of protein elasticity in vivo and in experimental setups, greatly reduces the attempt frequency with which the protein samples its free energy. Indeed, our data shows that a tethered polypeptide can traverse its free-energy landscape with a surprisingly low effective diffusion coefficient D_eff ∼ 1,200 nm²∕s. By contrast, our Molecular Dynamics simulations show that diffusion of an isolated protein under force occurs at D_eff ∼ 10⁸ nm²∕s, in agreement with fluorescence techniques measurements. This discrepancy is attributed to the drag force caused by the tethering object. From the physiological time scales of tissue elasticity, we calculate that tethered elastic proteins equilibrate in vivo with D_eff ∼ 10⁴–10⁶ nm²∕s which is two to four orders magnitude smaller than the values measured for untethered proteins in bulk.