Contractile signaling in the cell requires that the small GTPase RhoA recruit and engage downstream effectors at the plasma membrane. We now show that such signaling is conditioned by an intrinsically labile association of active, GTP-RhoA with the membrane. Effective signaling requires the scaffold anillin, which antagonizes the membrane-dissociation of GTP-RhoA independently of the canonical actions of GAPs and GDI. Anillin recruits GTP-RhoA by direct, reversible binding, and also locally concentrates PIP2 in the membrane. The latter functions to transiently enhance the membrane retention of free GTP-RhoA when it dissociates from anillin. Therefore cycles, where active RhoA first binds cortical anillin and then is retained by PIP2 even after disengagement, allow the dissociation kinetics of GTP-RhoA to be repeatedly ‘reset’, increasing its availability to recruit effectors. This demonstrates a new pathway for regulating contractile RhoA signalling and a more general model of scaffolding via the control of cortical dwell times. Further to this, we identified Myosin II as an anchor to concentrate Anillin at the cortex, thereby facilitating a positive feedback loop that can amplify signaling from RhoA for effective contractility.