Mechanisms controlling the expression of the electrically conductive pili (e-pili) of Geobacter species are of interest because of the important role of e-pili in diverse biogeochemical processes, anaerobic digestion and electromicrobiological applications. We investigated the function of the protein, designated Spc (short pilin chaperone), encoded by the gene immediately downstream from the gene for PilA, the monomer that assembles into e-pili. Multiple lines of evidence suggest that Spc forms an oligomer that is associated with the inner membrane. Mutating the start codon of spc to prevent translation increased the transcript abundance of pilA but greatly diminished the abundance of PilA, and e-pili could no longer be detected. Cross-linking, protein capture and two-hybrid studies demonstrated that Spc and PilA interacted. Two sites in PilA for electrostatic interaction with Spc were identified. The results demonstrate that Spc is required for PilA stability prior to incorporation into e-pili, suggesting that Spc has a chaperone function that may be specific to the relatively short PilA monomers that assemble into e-pili. These results are important for identifying microorganisms likely to express e-pili from (meta)genomic data and for the construction of microbial strains expressing e-pili.