Uropathogenic Escherichia coli (UPEC) cells can grow into highly filamentous forms during infection of bladder epithelial cells, but this process is poorly understood. Herein we found that some UPEC filaments released from infected bladder cells in vitro grew very rapidly and by more than 100 μm before initiating division, whereas others did not survive, suggesting that filamentation is a stress response that promotes dispersal. Looking at various cell division proteins using time-lapse fluorescence microscopy, we found that the normal division regulator FtsZ seem to need additional stabilisers to find proper division sites. The DamX bifunctional division protein, which is essential for UPEC filamentation, was initially non-localized but then assembled at multiple division sites in the filaments prior to division. Using single-molecule PALM microscopy we found that DamX rings maintained consistent thickness during constriction and remained at the septum until after membrane fusion was completed, like in rod cell division. Our findings suggest a mechanism involving regulated dissipation of DamX, leading to division arrest and filamentation, followed by its reassembly into division rings to promote UPEC dispersal and survival during infection.