Our understanding of bacterial cell size control is based mainly on stress-free growth conditions in the laboratory [1–10]. In the real world, however, bacteria are routinely faced with stresses that produce long filamentous cell morphologies [11–28]. Escherichia coli is observed to filament in response to DNA damage [22–25], antibiotic treatment [11–14, 28], host immune systems [15, 16], temperature [17], starvation [20], and more [18, 19, 21], conditions which are relevant to clinical settings and food preservation [26]. This shape plasticity is considered a survival strategy [27]. Size control in this regime remains largely unexplored. Here we report that E. coli cells use a dynamic size ruler to determine division locations combined with an adder-like mechanism to trigger divisions. As filamentous cells increase in size due to growth, or decrease in size due to divisions, its multiple Fts division rings abruptly reorganize to remain one characteristic cell length away from the cell pole and two such length units away from each other. These rules can be explained by spatiotemporal oscillations of Min proteins. Upon removal of filamentation stress, the cells undergo a sequence of division events, randomly at one of the possible division sites, on average after the time required to grow one characteristic cell size. These results indicate that E. coli cells continuously keep track of absolute length to control size, suggest a wider relevance for the adder principle beyond the control of normally sized cells, and provide a new perspective on the function of the Fts and Min systems. Wehrens, Ershov, et al. report a new size-control mechanism in E. coli cells that have elongated due to stress. Multiple division rings are continuously rearranged in response to growth and division to control daughter cell size when divisions resume. Divisions are spatially controlled by the Min system and temporally by the adder principle.@en