Protein export to the bacterial periplasm is achieved by SecYEG, an inner membrane heterotrimer. SecY and SecE are encoded by essential genes, while SecG is not essential for growth under standard laboratory conditions. Using a quantitative and sensitive export assay, we show that SecG plays a critical role for the residual export mediated by mutant signal sequences; the magnitude of this effect is not proportional to the strength of the export defect. In contrast, export mediated by wild-type signal sequences is only barely retarded in the absence of SecG. When probed with mutant signal sequences, secG loss of function mutations display a phenotype opposite to that of prlA mutations in secY. The analysis of secG and prlA single and double mutant strains shows that the increased export conferred by several prlA alleles is enhanced in the absence of SecG. Several combinations of prlA alleles with a secG deletion cannot be easily constructed. This synthetic phenotype is conditional, indicating that cells can adapt to the presence of both alleles. The biochemical basis of this phenomenon is linked to the stability of the SecYE dimer in solubilized membranes. With prlA alleles that can be normally introduced in a secG deletion strain, SecG has only a limited effect on the stability of the SecYE dimer. With the other prlA alleles, the SecYE dimer can often be detected only in the presence of SecG. A possible role for the maintenance of SecG during evolution is proposed.