Little is known about how Porphyromonas gingivalis, a Gram-negative oral anaerobe, senses environmental changes, and how such information is transmitted to the cell. The production of P. gingivalis surface fimbriae is regulated by FimS-FimR, a two component signal transduction system. Expression of fimA, encoding the fimbrilin protein subunit of fimbriae, is positively regulated by the FimR response regulator. In this study we investigated the molecular mechanisms of FimR regulation of fimA expression. Comparative transcription profiling of fimR wild-type and mutant strains shows that FimR controls the expression of several genes including five clustered around the fimA locus. Chromatin immunoprecipitation assays and electrophoretic mobility shift assays identify and confirm that FimR binds to the promoter region of the first gene in the fimA cluster. Gene expression analyses of mutant strains reveal a transcriptional cascade involving multiple steps, with FimR activating expression of the first gene of the cluster that encodes a key regulatory protein.