Intracellular bacterial pathogens often reprogram their mammalian host cells, including cell mechanical properties, to promote their own replication and spread. However, it is unclear whether mammalian host cells may modulate their biomechanics in response to infection in a way that would benefit the host by limiting bacterial infection. Inspired by this question, we monitored epithelial cell monolayers infected with low levels of Listeria monocytogenes. We found that, as the bacteria replicate and spread from cell to cell over several days, the infected host cells within the infection focus get progressively compressed by surrounding uninfected cells. Surrounding uninfected cells become highly polarized and move directionally towards the infection focus, squeezing the infected cells that eventually get extruded from the monolayer.Extruded cells continue adhering to the cellular monolayer, giving rise to a 3-dimensional (3D) mound of infected cells. We hypothesized that 3D mounding was driven by changes in the biomechanics of uninfected cells surrounding the mounds (surrounders) as well as the infected cells that eventually compose the mound (mounders). Indeed, we found that infected mounders, but not surrounders, become softer during infection and adhere more weakly on deformable matrices mimicking their natural environment. Through a combination of transcriptomics, pharmacological and genetic perturbations, we find that differentially upregulated innate immunity signaling, and downregulated cell-cell and cell-matrix adhesion pathways synergistically can drive the observed cellular competition between infected mounders and surrounders. Most importantly we find that activation of NF-κB is critical for mound formation, and show evidence that our findings extend to bacterial pathogens other than L. monocytogenes. Overall, our findings highlight the dynamic remodeling capability of epithelial tissue, and propose a novel biomechanical mechanism employed by host epithelial cells to eliminate bacterial infection.