Type IV Pili (T4Ps) are surface appendages used by gram-negative and gram-positive pathogens for adherence, biofilm formation, aggregation, and motility. In enteropathogenic Escherichia coli (EPEC), thirteen bundle-forming pilus (BFP) proteins are required and sufficient for pilus expression and function. This complex molecular machine has components in the cytoplasm, the inner-membrane (IM), the periplasm, and the outer-membrane (OM) that work in concert to polymerize monomers of bundlin, the major pilin subunit, into filaments. Little is known about the order of events that culminate in extension of the pilus fiber through the OM pore formed by the secretin protein, BfpB. To refine our understanding of BFP assembly, I isolated specific interactions between bundlin and additional BFP components. Using isothermal-titration calorimetry (ITC) and Förster Resonance Energy Transfer (FRET), we found that bundlin interacts with the periplasmic portion of the bitopic IM protein BfpC. Additional ITC experiments determined that bundlin also interacts with a periplasmic protein, BfpU. We confirmed that the interaction between bundlin and BfpU is soluble in the periplasm. We also utilized this interaction and a panel of bfp mutants to identify other BFP components that are required to extricate bundlin from the IM. Additionally, using Pseudomonas aeruginosa, we provide evidence that BfpU is a PilP homologue, as periplasmic PilP also interacts with the pilin monomer PilA. These results provide the first evidence for a soluble periplasmic stage in T4P biogenesis that occurs after pilin is extricated from the IM and prior to incorporation into pili. The final step of pilus biogenesis requires passage of the pilus filament through a secretin protein in the OM. Using biochemical labeling of specific BfpB residues and FRET, we mapped the topology of BfpB and propose that BfpB forms a beta barrel with 16 transmembrane beta strands. Surprisingly, the C-terminus of BfpB is extracellular, a result confirmed by flow cytometry for BfpB and a distantly related T4P secretin, PilQ, from P. aeruginosa. These experiments expand our knowledge on steps that occur during pilus biogenesis, highlighting new protein-protein interactions. Additionally we provide new and comprehensive information on the topology of a T4P secretin.