Plants respond to limiting concentrations of inorganic phosphate (Pi) in the environment by activating a phosphate starvation response (PSR). PSR encompasses a complex array of transcriptional responses, manifested in morphological, developmental, and physiological changes. As PSR was originally described under sterile conditions, the relevance of these findings to realistic environmental conditions is unknown because plant roots are intimately associated with microbial communities. These communities and their interactions with the plant can range from competition to cooperation depending, among other factors, on the nutrient content of the surrounding soil. In order to study the interplay between induction of PSR and plant-microbe interactions under limiting Pi conditions, we used a ‘split-root’ assay in which Arabidopsis thaliana roots were divided across two sides of an agar plate differing in Pi concentrations and in the inoculation of a 35-member synthetic bacterial community (SynCom). The induction of PSR in the plant was measured using a reporter system that expresses β-glucuronidase (GUS) under the control of the IPS1 promoter, which is strongly induced at low Pi. We found that high Pi in one compartment repressed bacterially-induced PSR in the adjacent low Pi compartment, indicating that regulation of signaling in bacterially-triggered PSR is systemic. PSR induced by bacteria has common regulatory and signaling elements with the canonical PSR that occurs in sterile conditions, and could serve as a model for studying the mechanisms of PSR induction in nature. Plants grown with bacteria increased Pi accumulation in Pi-replete media compared to plants grown in sterile conditions. We observed clear bacterial community shifts between the plant and the agar, and several strains significantly changed in relative abundance in response to direct and plant-mediated effects of Pi concentration, suggesting that systemic PSR-related signals are both induced by bacteria and affect them.