Assembly of the cytoskeletal protein FtsZ into a ring-like structure is required for bacterial cell division. Structurally, FtsZ consists of four domains: the globular N-terminal core, a flexible linker, 8–9 conserved residues implicated in interactions with modulatory proteins, and a highly variable set of 4–10 residues at its very C terminus. Largely ignored and distinguished by lack of primary sequence conservation, the linker is presumed to be intrinsically disordered. Here we employ genetics, biochemistry and cytology to dissect the role of the linker in FtsZ function. Data from chimeric FtsZs substituting the native linker with sequences from unrelated FtsZs as well as a helical sequence from human beta-catenin indicate that while variations in the primary sequence are well tolerated, an intrinsically disordered linker is essential forBacillus subtilisFtsZ assembly. Linker lengths ranging from 25 to 100 residues supported FtsZ assembly, but replacing theB. subtilisFtsZ linker with a 249-residue linker fromAgrobacterium tumefaciensFtsZ interfered with cell division. Overall, our results support a model in which the linker acts as a flexible tether allowing FtsZ to associate with the membrane through a conserved C-terminal domain while simultaneously interacting with itself and modulatory proteins in the cytoplasm.