Fiber units are conserved design motifs that bestow intrinsic stiffness to biological tissues. Collagen fibrils are the fundamental unit of fibrous tissues with controlled assembly and multiscale structure‐function properties. Characteristic non‐linear tissue response is afforded through energy dissipation at the stiff‐soft interfaces of fibril collagen and extrafibrillar matrix components. The goal of this research is to develop a 3D silk hydrogel microfiber platform with bioinspired toughening mechanisms. Batch fabrication and post‐processing renders fibers that can be handled and with tunable features, as well as loading of components to improve material responses. Matrix loading of a glycoprotein, bovine serum albumin (BSA), adds a primary defense mechanism to material failure in the form of sacrificial bonds. This enables nano‐ to micro‐scale rearrangement with strain and improved fiber toughness compared to silk‐only fibers. Further biomimicry is added via matrix loading of a biosilica precursor peptide, R5, enabling biomineralization in the form of silicification. Inorganic mineral deposition of Silk‐BSA‐R5 hydrogel microfibers provides a fibrous scaffold for applications that require fibril‐mineral interfaces for load transduction. This microfiber platform introduces a methodology for meticulous fibrous scaffold design with biomimetic fibril hierarchy, toughening mechanisms, and loading capabilities for systematic tissue engineering applications.