Phosphate represents a major limiting factor for plant productivity. Plants have evolved different solutions to adapt to phosphate limitation ranging from a profound tuning of their root system architecture and metabolic profile to the evolution of widespread mutualistic interactions. Here we elucidated plant responses and their genetic basis to different phosphate levels in a plant species that is widely used as a model for AM symbiosis: Lotus japonicus. Rather than focussing on a single model strain, we measured root growth and anion content in response to different levels of phosphate in 130 Lotus natural accessions. This allowed us not only to uncover common as well as divergent responses within this species, but also enabled Genome Wide Association Studies by which we identified new genes regulating phosphate homeostasis in Lotus. Among them, we showed that insertional mutants of a cytochrome B5 reductase and a Leucine-Rich-Repeat receptor showed different phosphate concentration in plants grown under phosphate sufficient condition. Under low phosphate conditions, we found a correlation between plant biomass and the decrease of plant phosphate concentration in plant tissues, representing a dilution effect. Altogether our data of the genetic and phenotypic variation within a species capable of AM complements studies that have been conducted in Arabidopsis, and advances our understanding of the continuum of genotype by phosphate level interaction existing throughout dicot plants.