Phosphate (P(i)) is a major limiting factor for plant growth. Plants respond to limiting P(i) supplies by inducing a suite of adaptive responses comprising altered growth behaviour, enhanced P(i) acquisition and reduced P(i) demand that together define a distinct physiological state. In P(i)-starved plants, continued root growth is required for P(i) acquisition from new sources, yet meristem activity consumes P(i). Therefore, we analysed the relationship between organ growth, phosphate starvation-responsive (PSR) gene expression and P(i) content in Arabidopsis thaliana under growth-promoting or inhibitory conditions. Induction of PSR gene expression after transfer of plants to P(i)-depleted conditions quantitatively reflects prior levels of P(i) acquisition, and hence is sensitive to the balance of P(i) supply and demand. When plants are P(i)-starved, enhanced root or shoot growth exacerbates, whereas growth inhibition suppresses, P(i) starvation responses, suggesting that the magnitude of organ growth activity specifies the level of P(i) demand. Inhibition of cell-cycle activity, but not of cell expansion or cell growth, reduces P(i) starvation-responsive gene expression. Thus, the level of cell-cycle activity specifies the magnitude of P(i) demand in P(i)-starved plants. We propose that cell-cycle activity is the ultimate arbiter for P(i) demand in growing organs, and that other factors that influence levels of PSR gene expression do so by affecting growth through modulation of meristem activity.