The process of self-assembly of protein subunits in complex shaped supramolecular structures is not well understood. Silicatein proteins are involved in the biogenic synthesis of glass in marine sponges. As multi-subunit macroscopic filaments they apparently act both as a catalyst and template controlling the synthesis of silica needles in the Demospongia. Self-assembly of the silicatein monomers and oligomers is shown to form fibrous structures by a mechanism fundamentally different from any previously described filament assembly process. This assembly proceeds through the formation of diffusion-limited fractally patterned aggregates on the path to filament formation. The driving force for this self-assembly is suggested to be entropic, mediated by the interaction of hydrophobic patches on the surfaces of the silicatein subunits that are not found on highly homologous congeners that do not form filaments. These results are consistent with a model wherein silicatein monomers associate into oligomers stabilized by intermolecular disulfide bonds. The oligomeric units assemble into a fractal network that subsequently condenses and organizes into a filamentous structure. Evidence from fiber diffraction studies confirms previous suggestions that the native silicatein filament structure has crystalline order with hexagonal packing. A mechanistic pathway whereby the two-dimensional protein sheet formed by the fractal intermediates self-assemble "accordion-style" into a well-ordered protein filament is proposed. Computational modeling based on the entropic and Brownian instability in such dynamical systems supports this hypothesis, accounting for the self-assembly of the filament with a hexagonal (frustrated triangular) cross section. This presents a new paradigm for understanding how organisms make large arrays of highly ordered proteins while maintaining control of the assembly processes.