The root system architecture is crucial to adapt plant growth to changing soil environmental conditions and consequently to maintain crop yield. In addition to root branching through lateral roots, legumes can develop another organ, the nitrogen-fixing nodule, upon a symbiotic bacterial interaction. A mutant, cra1, showing compact root architecture was identified in the model legume Medicago truncatula. cra1 roots were short and thick due to defects in cell elongation, whereas densities of lateral roots and symbiotic nodules were similar to the wild type. Grafting experiments showed that a lengthened life cycle in cra1 was due to the smaller root system and not to the pleiotropic shoot phenotypes observed in the mutant. Analysis of the cra1 transcriptome at a similar early developmental stage revealed few significant changes, mainly related to cell wall metabolism. The most down-regulated gene in the cra1 mutant encodes a Caffeic Acid O-Methyl Transferase, an enzyme involved in lignin biosynthesis; accordingly, whole lignin content was decreased in cra1 roots. This correlated with differential accumulation of specific flavonoids and decreased polar auxin transport in cra1 mutants. Exogenous application of the isoflavone formononetin to wild-type plants mimicked the cra1 root phenotype, whereas decreasing flavonoid content through silencing chalcone synthases restored the polar auxin transport capacity of the cra1 mutant. The CRA1 gene, therefore, may control legume root growth through the regulation of lignin and flavonoid profiles, leading to changes in polar auxin transport.