White lupin (Lupinus albus L.) is a legume that produces seeds recognized for their high protein content and good nutritional value (lowest glycemic index of all grains, high dietary fiber content, and zero gluten or starch)1–5. White lupin can form nitrogen-fixing nodules but has lost the ability to form mycorrhizal symbiosis with fungi6. Nevertheless, its root system is well adapted to poor soils: it produces cluster roots, constituted of dozens of determinate lateral roots that improve soil exploration and phosphate remobilization7. As phosphate is a limited resource that comes from rock reserves8, the production of cluster roots is a trait of interest to improve fertilizers efficiency. Using long reads sequencing technologies, we provide a high-quality genome sequence of a modern variety of white lupin (2n=50, 451 Mb), as well as de novo assemblies of a landrace and a wild relative. We describe how domestication impacted soil exploration capacity through the early establishment of lateral and cluster roots. We identify the APETALA2 transcription factor LaPUCHI-1, homolog of the Arabidopsis morphogenesis coordinator9, as a potential regulator of this trait. Our high-quality genome and companion genomic and transcriptomic resources enable the development of modern breeding strategies to increase and stabilize yield and to develop new varieties with reduced allergenic properties (caused by conglutins10), which would favor the deployment of this promising culture.