Summary Modern agriculture needs large quantities of phosphate (Pi) fertilisers to obtain high yields. Information on how plants sense and adapt to Pi is required to enhance phosphorus‐use efficiency (PUE) and thereby promote agricultural sustainability. Here, we show that strigolactones (SLs) regulate rice root developmental and metabolic adaptations to low Pi, by promoting efficient Pi uptake and translocation from roots to shoots. Low Pi stress triggers the synthesis of SLs, which dissociate the Pi central signalling module of SPX domain‐containing protein (SPX4) and PHOSPHATE STARVATION RESPONSE protein (PHR2), leading to the release of PHR2 into the nucleus and activating the expression of Pi‐starvation‐induced genes including Pi transporters. The SL synthetic analogue GR24 enhances the interaction between the SL receptor DWARF 14 (D14) and a RING‐finger ubiquitin E3 ligase (SDEL1). The sdel mutants have a reduced response to Pi starvation relative to wild‐type plants, leading to insensitive root adaptation to Pi. Also, SLs induce the degradation of SPX4 via forming the D14‐SDEL1‐SPX4 complex. Our findings reveal a novel mechanism underlying crosstalk between the SL and Pi signalling networks in response to Pi fluctuations, which will enable breeding of high‐PUE crop plants.