In plants, where cells cannot migrate, asymmetric cell divisions (ACDs) must be confined to the appropriate spatial context. We investigate tissue-generating asymmetric divisions in a stem cell daughter within the Arabidopsis root. Spatial restriction of these divisions requires physical binding of the stem cell regulator SCARECROW (SCR) by the RETINOBLASTOMA-RELATED (RBR) protein. In the stem cell niche, SCR activity is counteracted by phosphorylation of RBR through a cyclinD6;1-CDK complex. This cyclin is itself under transcriptional control of SCR and its partner SHORT ROOT (SHR), creating a robust bistable circuit with either high or low SHR-SCR complex activity. Auxin biases this circuit by promoting CYCD6;1 transcription. Mathematical modeling shows that ACDs are only switched on after integration of radial and longitudinal information, determined by SHR and auxin distribution, respectively. Coupling of cell-cycle progression to protein degradation resets the circuit, resulting in a “flip flop” that constrains asymmetric cell division to the stem cell region. Display omitted ► SCR binds its partner SHR to stimulate together with auxin CyclinD6 transcription ► CyclinD6 inactivates RBR, but RBR binds and inactivates SCR, blocking CyclinD6 ► This bistable switch interprets multiple gradients to trigger stem cell division ► Protein degradation is used to bring daughter cells back to an “off” state Stem cells in the root meristem integrate radial and longitudinal gradients of tissue patterning determinants to ensure that only specific stem cells undergo asymmetric cell divisions.