Polar localization of proteins in the Caulobacter predivisional cell results in the formation of two distinct progeny cells, a motile swarmer cell and a sessile stalked cell. The transcription of several flagellar promoters is localized to the swarmer pole of the predivisional cell. We present evidence that the product of the flbD gene is the transcriptional activator of these promoters. We show that FlbD is distributed in all cell types and in both poles of the predivisional cell. We also demonstrate that FlbD can be phosphorylated, and that a FlbD kinase activity is under cell cycle control. Cells expressing a FlbD mutant that should activate transcription in the absence of phosphorylation, exhibited an alteration in the temporal pattern of flagellin transcription. Furthermore, predivisional cells expressing the mutant FlbD failed to polarly localize flagellin synthesis. We propose that the phosphorylation of FlbD is restricted to the swarmer compartment of the predivisional cell, and serves as the control point for regulating the spatial transcription of flagellar promoters.