The RNA-binding protein CsrA regulates the expression of hundreds of genes in several bacterial species, thus controlling virulence and other processes. However, the outcome of the CsrA-mRNA interactions is modulated by competing small RNAs and other factors through mechanisms that are only partially understood. Here, we show that CsrA accumulates in a dynamic membraneless compartment in cells of E. coli and other pathogenic species. In addition to CsrA, the compartment contains components of the RNA-degrading complex (degradosome), regulatory small RNAs, and selected mRNAs. Formation of the compartment is associated with a switch between promoting and repressing virulence gene expression by CsrA. We suggest that similar CsrA switches may be widespread in diverse bacteria.