Phosphate (Pi) deficiency remains a significant challenge in agricultural soils worldwide, profoundly impacting plant growth and crop yield. Pi deficiency affects legumes, drastically reducing nodule formation and hampering nitrogen fixation and overall plant productivity. Despite considerable progress in understanding how legumes adapt to Pi deficiency during symbiotic interactions with rhizobia, the genetic mechanisms orchestrating this symbiosis under Pi-limiting conditions remain elusive. Ignoring the low Pi problem not only compromises the functionality of the nitrogen cycle by nitrogen fixation through legumes but can also put food security at risk globally. Hence, it is imperative to understand the genetic mechanisms underlying the establishment of the root nodule symbiosis under low Pi conditions. Here, we present experimental evidence supporting that part of the Autoregulation of Nodulation (AON) pathway and the transcription factor Phosphate Starvation Response (PHR) are key genetic regulators of the root nodule symbiosis under Pi-limiting conditions. Furthermore, we present evidence that the transcriptional activity of Nodule Inception (NIN), the master regulator of the root nodule symbiosis, is modulated according to the plant host’s Pi status. The knowledge generated until now is paving the road to better harness the ecological services of the root nodule symbiosis even under Pi-deficient conditions, offering hope for improved agricultural productivity and food security.