Biomaterials synthesized from cross-linked folded proteins have untapped potential for biocompatible, resilient, and responsive implementations, but face challenges due to costly molecular refinement and limited understanding of their mechanical response. Under a stress vector, these materials combine the gel-like response of cross-linked networks with the mechanical unfolding and extension of proteins from well-defined 3D structures to unstructured polypeptides. Yet the nanoscale dynamics governing their viscoelastic response remains poorly understood. This lack of understanding is further exacerbated by the fact that the mechanical stability of protein domains depends not only on their structure, but also on the direction of the force vector. To this end, here we propose a coarse-grained network model based on the physical characteristics of polyproteins and combine it with the mechanical unfolding response of protein domains, obtained from single molecule measurements and steered molecular dynamics simulations, to explain the macroscopic response of protein-based materials to a stress vector. We find that domains are about 10-fold more stable when force is applied along their end-to-end coordinate than along the other tethering geometries that are possible inside the biomaterial. As such, the macroscopic response of protein-based materials is mainly driven by the unfolding of the node-domains and rearrangement of these nodes inside the material. The predictions from our models are then confirmed experimentally using force-clamp rheometry. This model is a critical step toward developing protein-based materials with predictable response and that can enable applications for shape memory and energy storage and dissipation.