Summary Phosphate (Pi) is a critical macronutrient for the biochemical and molecular functions of cells. Under phosphate limitation, plants manifest adaptative strategies to increase phosphate scavenging. However, how low phosphate sensing links to the transcriptional machinery remains unknown. The role of the MEDIATOR (MED) transcriptional co‐activator, through its MED16 subunit in Arabidopsis root system architecture remodeling in response to phosphate limitation was assessed. Its critical function acting over the SENSITIVE TO PROTON RHIZOTOXICITY1 (STOP1)‐ALUMINUM‐ACTIVATED MALATE TRANSPORT1 (ALMT1) signaling module was tested through a combination of genetic, biochemical, and genome‐wide transcriptomic approaches. Root system configuration in response to phosphate scarcity involved MED16 functioning, which modulates the expression of a large set of low‐phosphate‐induced genes that respond to local and systemic signals in the Arabidopsis root tip, including those directly activated by STOP1. Biomolecular fluorescence complementation analysis suggests that MED16 is required for the transcriptional activation of STOP1 targets, including the membrane permease ALMT1, to increase malate exudation in response to low phosphate. Our results unveil the function of a critical transcriptional component, MED16, in the root adaptive responses to a scarce plant macronutrient, which helps understanding how plant cells orchestrate root morphogenesis to gene expression with the STOP1‐ALMT1 module.