Iron (Fe) and phosphate (Pi) are two essential nutrients that are poorly available in the soil and should be supplemented either as fertilizers or organic amendments to sustain crop production. Currently, determining how rhizosphere bacteria contribute to plant mineral nutrient acquisition is an area of growing interest regarding its potential application in agriculture. The aim of this study was to investigate the influence of root colonization by Pseudomonas putida for Arabidopsis growth through Fe and Pi nutritional signaling. We found that root colonization by the bacterium inhibits primary root elongation and promotes the formation of lateral roots. These effects could be related to higher expression of two Pi starvation-induced genes and AtPT1, the major Pi transporter in root tips. In addition, P. putida influenced the accumulation of Fe in the root and the expression of different elements of the Fe uptake pathway. The loss of function of the protein ligase BRUTUS (BTS), and the bHLH transcription factors POPEYE (PYE) and IAA-LEUCINE RESISTANT3 (ILR3) compromised the root branching stimulation triggered by bacterial inoculation while the leaf chlorosis in the fit1 and irt1–1 mutant plants grown under standard conditions could be bypassed by P. putida inoculation. The WT and both mutant lines showed similar Fe accumulation in roots. P. putida repressed the expression of the IRON-REGULATED TRANSPORTER 1 (IRT1) gene suggesting that the bacterium promotes an alternative Fe uptake mechanism. These results open the door for the use of P. putida to enhance nutrient uptake and optimize fertilizer usage by plants.