Helicobacter pylori is a significant human pathogen that infects a large percentage of the worldwide population with infections potentially resulting in acute gastritis, peptic ulcers, gastric carcinoma and non-Hodgkin lymphoma. Many essential H. pylori colonization factors have been identified including flagellar motility. Flagellar biosynthesis requires over 40 proteins and all three sigma factors (RpoD, RpoN and FliA) in the cell. Transcription of the H. pylori RpoN regulon is controlled by the FlgS/FlgR two-component regulatory system which responds to undefined cellular cues. Previous studies showed that expression of the RpoN- and FliA-dependent flagellar genes is linked to a functional flagellar protein export apparatus. FlhB, a membrane-bound component of the export apparatus, has a large cytoplasmic domain (FlhBC) which is processed by a site-specific autocleavage. FlhBC processing accompanies a switch in substrate specificity of the export apparatus. To determine if processing of FlhB influenced flagellar gene expression, two mutations at the cleavage site in FlhB were constructed. Both substitutions inhibited autocleavage of FlhB as well as motility. The mutants were able to export rod-/hook-type substrates but not filament-type substrates. The FlhB variant strains expressed RpoN- and FliA-dependent reporter genes at wild-type levels. Disruption of the hook length control protein FliK in the FlhB variant strains had different consequences for expression of the reporter genes suggesting that FliK has different effects on the export apparatus depending on the conformation of FlhB. Disruption of fliK in a flhB mutant did not restore expression of RpoN-dependent reporter genes indicating that failure to export FliK does not account for inhibition of the RpoN regulon in export apparatus mutants. FlhA, another membrane-bound component of the export apparatus, also has a large cytoplasmic domain. Specific flhA insertion mutations stimulated expression of RpoN-dependent reporter genes. These flhA mutants are deficient in motility and export of both rod-/hook-type and filament-type substrates confirming that the export apparatus is not required for export of an inhibitor of the RpoN regulon. Taken together, these results support a model in which FlgS directly or indirectly senses the conformation of the export apparatus.