The Type III secretion system (T3SS) is used by Gram-negative bacteria, including important pathogens, to manipulate eukaryotic target cells by injecting effector proteins. T3SS secretion is tightly regulated and accompanied by a phenomenon called secretion-associated growth inhibition (SAGI). Since actively secreting bacteria cannot grow and divide, a non-uniform distribution of T3SS expression is conceivably beneficial during infection. Yersinia enterocolitica, a main T3SS model organism that uses the system to evade the host immune response, had so far been found to uniformly express and assemble T3SSs, which are then activated by target cell contact. However, in this study, we found that Yersinia actively suppress T3SS expression, assembly and activity at higher cell densities, such as inside microcolonies. This effect is highly specific to the T3SS, reversible, and distinct from stationary phase adaptation. It is conferred by the T3SS transcriptional activator VirF, which is downregulated at the higher cell densities and whose in trans expression restores T3SS assembly and activity. Transcript analysis showed that this effect is mediated by increased levels of the regulatory RNAs CsrBC, which sequester the regulatory protein CsrA and destabilize the virF transcript. Cell adhesion, an essential trait for Yersinia virulence, linked to T3SS secretion and regulated by VirF also showed to be affected by local higher cell densities. The concomitant downregulation of the VirF-dependent adhesin YadA led to a drastic reduction in bacterial cell adhesion. We propose that this active suppression of T3SS secretion and cell attachment at higher local bacterial densities promotes a switch during Yersinia infection from a T3SS-active colonization stage to a bacterial replication and dissemination phase.