Lateral root (LR) formation is governed by a complex regulatory network that includes various internal factors such as transcription factors (TFs) and phytohormones, of which ethylene is a key repressor. However, the core TFs that regulate ethylene biosynthesis and LR development remain unknown. Here, we found that the WRKY TF SbWRKY50 was required for LR development in Sorghum bicolour L. Overexpression of SbWRKY50 in sorghum increased the number and length of LRs, whereas both decreased in the CRISPR/Cas9-edited SbWRKY50 mutant. SbWRKY50 positively regulated LR generation by directly repressing several 1-aminocyclopropane-1-carboxylate synthase (ACS) genes. In addition, SbWRKY50 directly interacted with SbBMI1A to facilitate the recruitment of the PRC1 complex and induced H2A ubiquitination (H2Aub) accumulation on SbACS genes, thereby promoting epigenetic silencing and LR formation. The positive role of SbWRKY50 in stay-green and LR formation improves the agronomic traits of sorghum, improving drought tolerance and potentially contributing to increased sorghum yield.