As part of our attempt to map the impact of acetyl phosphate (acetyl∼P) on the entire network of two-component signal transduction pathways in Escherichia coli, we asked whether the influence of acetyl∼P on capsular biosynthesis and flagellar biogenesis depends on the Rcs phosphorelay. To do so, we performed a series of epistasis experiments: mutations in the components of the pathway that controls acetyl∼P levels were combined with mutations in components of the Rcs phosphorelay. Cells that did not synthesize acetyl∼P produced no capsule under normally permissive conditions, while those that accumulated acetyl∼P synthesized capsule under conditions previously considered to be non-permissive. Acetyl∼P-dependent capsular biosynthesis required both RcsB and RcsA, while the lack of RcsC restored capsular biosynthesis to acetyl∼P-deficient cells. Similarly, acetyl∼P-sensitive repression of flagellar biogenesis was suppressed by the loss of RcsB (but not of RcsA), while it was enhanced by the lack of RcsC. Taken together, these results show that both acetyl∼P-sensitive activation of capsular biosynthesis and acetyl∼P-sensitive repression of flagellar biogenesis require the Rcs phosphorelay. Moreover, they provide strong genetic support for the hypothesis that RcsC can function as either a kinase or a phosphatase dependent on environmental conditions. Finally, we learned that RcsB and RcsC inversely regulated the timing of flagellar biogenesis: rcsB mutants elaborated flagella prematurely, while rcsC mutants delayed their display of flagella. Temporal control of flagella biogenesis implicates the Rcs phosphorelay (and, by extension, acetyl∼P) in the transition of motile, planktonic individuals into sessile biofilm communities.