The peptidoglycan cell wall is a hallmark of the bacterial subkingdom. Surprisingly, many modern bacteria retain the ability to switch into a wall-free state called the L-form. L-form proliferation is remarkable in being independent of the normally essential FtsZ-based division machinery and in occurring by membrane blebbing and tubulation. We show that mutations leading to excess membrane synthesis are sufficient to drive L-form division in Bacillus subtilis. Artificially increasing the cell surface area to volume ratio in wild-type protoplasts generates similar shape changes and cell division. Our findings show that simple biophysical processes could have supported efficient cell proliferation during the evolution of early cells and provide an extant biological model for studying this problem.