Bacteria switch the direction their flagella rotate to control movement. FliM, along with FliN and FliG, compose a complex in the motor that, upon binding phosphorylated CheY, reverses the sense of flagellar rotation. The 2.0-A resolution structure of the FliM middle domain (FliM(M)) from Thermotoga maritima reveals a pseudo-2-fold symmetric topology similar to the CheY phosphatases CheC and CheX. A variable structural element, which, in CheC, mediates binding to CheD (alpha2') and, in CheX, mediates dimerization (beta'(x)), has a truncated structure unique to FliM (alpha2'). An exposed helix of FliM(M) (alpha1) does not contain the catalytic residues of CheC and CheX but does include positions conserved in FliM sequences. Cross-linking experiments with site-directed cysteine mutants show that FliM self-associates through residues on alpha1 and alpha2'. CheY activated by BeF(3)(-) binds to FliM with approximately 40-fold higher affinity than CheY (K(d) = 0.04 microM vs. 2 microM). Mapping residue conservation, suppressor mutation sites, binding data, and deletion analysis onto the FliM(M) surface defines regions important for contacts with the stator-interacting protein FliG and for either counterclockwise or clockwise rotation. Association of 33-35 FliM subunits would generate a 44- to 45-nm-diameter disk, consistent with the known dimensions of the C-ring. The localization of counterclockwise- and clockwise-biasing mutations to distinct surfaces suggests that the binding of phosphorylated CheY cooperatively realigns FliM around the ring.