Staphylocoagulase (SC), a crucial virulence protein secreted by several strains of the major pathogen , functions as a potent inducer of blood clotting. SC binds its zymogen target, prothrombin (ProT) with subnanomolar affinity, allosterically inducing a thrombin-like active site in the bound zymogen. The resulting SC·(Pro)T* active complexes effectively convert fibrinogen (Fbg) into clot-forming fibrin (Fbn). We previously reported crystal structures of the N-terminal SC domains, responsible for ProT binding and activation, and characterized the mechanism of cofactor-induced zymogen activation in detail. However, the lack of three-dimensional (3D) structures for the C-terminal SC region has hampered a complete understanding of its role in Fbg recognition and cleavage. Here, we present and discuss 3D models of the Fbg-binding SC region. Our results suggest that the major C-terminal domain of SC folds into a single-layer β-sheet structurally similar to the membrane occupation and recognition nexus (MORN) family of tandem repeats. We further propose a folding pathway for this C-terminal SC region that is contingent upon the presence of its substrate, Fbg. These structural and mechanistic insights are critical for understanding SC-mediated fibrin generation, which is highly relevant to heart valve vegetations and biofilm formation during infection.