Stem cells must balance self-renewal and differentiation; thus, their activities are precisely controlled. In plants, the control circuits that underlie division and differentiation within meristems have been well studied, but those that underlie feedback on meristems from lateral organs remain largely unknown. Here we show that long-distance auxin transport mediates this feedback in a non-cell-autonomous manner. A low-auxin zone is associated with the shoot apical meristem (SAM) organization center, and auxin levels negatively affect SAM size. Using computational model simulations, we show that auxin transport from lateral organs can inhibit auxin transport from the SAM through an auxin transport switch and thus maintain SAM auxin homeostasis and SAM size. Genetic and microsurgical analyses confirmed the model’s predictions. In addition, the model explains temporary change in SAM size of yabby mutants. Our study suggests that the canalization-based auxin flux can be widely adapted as a feedback control mechanism in plants.