Plant root development is tightly regulated in plants to optimize nutrient acquisition and interactions with soil microorganisms. In legumes, the Autoregulation of Nodulation (AoN) pathway systemically controls the proliferation of root nodules, which are energy-intensive organs. Mutations affecting the AoN pathway result in a hypernodulation phenotype accompanied by altered root development; however, it remains unclear whether this regulation of root development is systemic and coordinated with nodulation. Through a forward genetic screen, we identified the constitutive cluster root 1 (ccr1) mutant in white lupin (Lupinus albus), which exhibits constitutive production of an excessive number of cluster roots. We demonstrate that CCR1 is the ortholog of the Medicago truncatula SUNN leucin-rich repeat-receptor like kinase (LRR-RLK), a key regulator of the AoN pathway and that CCR1 negatively regulates both nodule and cluster root development via a common shoot-to-root signaling pathway. Interspecific grafting experiments between white and narrow-leaved lupin (Lupinus angustifolius), a species incapable of producing cluster roots, show that ccr1 shoots can induce the formation of cluster-like roots in narrow-leaved lupin rootstocks, highlighting the conservation of the CCR1-dependent inhibitory signaling cascade. Transcriptomic analyses reveal that CCR1 targets the conserved regulatory module NIN/LBD16-NFYA, which connects nodule and lateral root developmental through a shared inhibitory systemic pathway. We propose that this pathway represents a broader developmental control mechanism, termed Autoregulation of Development (AoDev).