Neisseria gonorrhoeae (Gc) is the causative agent of the sexually transmitted infection gonorrhea. During pathogenesis, N. gonorrhoeae uses Type IV pili (T4p) to adhere to host cells and promote colonization. T4p are dynamic structures made of pilin fibers that extend and retract from the bacterial cell. Beyond host cell adhesion, T4p are involved in a variety of cellular processes including DNA uptake, twitching motility, and resistance to antimicrobial agents. We previously identified a novel component of the N. gonorrhoeae T4p, which we named TfpC. Our published data illustrated that TfpC is required for full piliation, as a TfpC loss-of-function mutant has fewer pili. Full piliation is restored in the absence of both TfpC and the PilT retraction ATPase. Here, we use genetic, biochemical, and biophysical techniques to define how TfpC contributes to T4p dynamics and architecture. Using structure-function approaches, we evaluate the contribution of TfpC’s unique structure to its role in maintaining a subset of pili and define key residues needed for protein stability and function. Moreover, we will explain the interactions between TfpC and other T4p components. These studies expand our current understanding of T4p architecture as well as the components governing mechanisms of T4p extension and retraction.