The class of proteins collectively known as periplasmic immunoglobulin‐like chaperones play an essential role in the assembly of a diverse set of adhesive organelles used by pathogenic strains of Gram‐negative bacteria. Herein, we present a combination of genetic and structural data that sheds new light on chaperone–subunit and subunit–subunit interactions in the prototypical P pilus system, and provides new insights into how PapD controls pilus biogenesis. New crystallographic data of PapD with the C‐terminal fragment of a subunit suggest a mechanism for how periplasmic chaperones mediate the extraction of pilus subunits from the inner membrane, a prerequisite step for subunit folding. In addition, the conserved N‐and C‐terminal regions of pilus subunits are shown to participate in the quaternary interactions of the mature pilus following their uncapping by the chaperone. By coupling the folding of subunit proteins to the capping of their nascent assembly surfaces, periplasmic chaperones are thereby able to protect pilus subunits from premature oligomerization until their delivery to the outer membrane assembly site.