The Type 3 Secretion System (T3SS) is a mega-Dalton-scale bacterial organelle functioning as a molecular syringe that injects proteins directly into eukaryotic cells. Several important pathogens utilise this system as a virulence factor and as it features a surface-presenting ‘needle tip complex’, the T3SS is an attractive candidate as a therapeutic target or antigen. The massive, multi-component structure of the T3SS, and its all-or-nothing assembly presents both challenges to its study as well as an opportunity to better understand how molecular interactions can scale to form larger structures. We employ an engineering approach to understanding molecular structures; by re-building biological complexes from the bottom up and probing assembly structure and kinetics in the process. Integrating current structural knowledge, we form a ‘biological blueprint’ of the T3SS tip complex and using DNA nanotechnology, we have designed and synthesized molecular scaffolds to direct the arrangement and stoichiometry of protein subunits as is laid out in the blueprint. We present TEM and solution X-ray scattering structures of DNA templates and the tip complex proteins, supramolecular and covalent attachment of proteins to DNA, and the kinetics of T3SS tip complex proteins assembling on DNA scaffolds. By assembling parts of large protein structures in vitro, the context of subunits in-situ may be retained whilst permitting measurements of structure and kinetics that were previously confounded by the larger whole. The precise control afforded by DNA nanotechnology also expands the scope of manipulation of the assembly conditions to experiment with and presents the possibility of engineering novel protein assemblies for applied use.