The LuxR-type transcriptional regulator OryR of the rice pathogen Xanthomonas oryzae pv. oryzae (Xoo) is a member of a subgroup of regulators found in plant-associated bacteria that are known to respond to plant signals. OryR has been shown previously to positively regulate the neighbouring pip gene and to be important for rice virulence. The role of this inter-kingdom signalling regulator was investigated through a genome-wide transcriptome analysis. OryR was found to positively regulate 220 genes, whereas 110 were down-regulated. A significant over-representation of movement-related genes among the positively regulated ones was found, including 30 flagellar genes, accounting for 14% of the up-regulated genes above the two-fold cut-off value. In Xoo, both swimming and swarming respond to rice macerate and OryR plays a role in the induction of both of these types of motility under these conditions. In this study, we have also shown that the flagellar regulator flhF contains a lux box-like element in its promoter region, similar to the oryR-regulated neighbouring pip gene; via the use of a transcriptional fusion reporter, it was shown that flhF is regulated by OryR. Finally, the role of OryR in motility was also demonstrated by the significant reduction in flagellin content in the oryR Xoo mutant with respect to the wild-type, as observed by in planta proteomics studies.