The flagellum is a complex surface structure necessary for a number of activities including motility, chemotaxis, biofilm formation and host attachment. Flagellin, the primary structural protein making up the flagellum, is an abundant and potent activator of innate and adaptive immunity and therefore expression of flagellin during infection could be deleterious to the infection process due to flagellin-mediated host recognition. Herein, we demonstrate that in the fish pathogen Yersinia ruckeri the flagellin gene (fliC) is repressed during infection and subsequently de-repressed upon host death when tested in rainbow trout. These results suggests that Y. ruckeri possesses a regulatory system capable of sensing live host and modulating the expression of motility in response. Examination of the master flagellar operon (flhDC) promoter region revealed potential interaction with the Rcs pathway through an Rcs(A)B Box. Deletion of rcsB (rcsB?) resulted in overproduction of flagellin and unregulated motility, showing that the Rcs pathway negatively regulates biosynthesis of the flagellar apparatus. Experimental challenge with rcsB? and rcsB?fliC?? mutants revealed that mutation of the Rcs pathway results in virulence attenuation which is dependent on presence of the flagellin gene. These results suggest that the inappropriate expression of flagellin during infection triggers host recognition and thus immune stimulation resulting in attenuation of virulence. In addition, RNAseq analyses of the rcsB? mutant strain verified the role of this gene as a negative regulator of the flagellar motility system and identified several additional genes regulated by the Rcs pathway.