Propagation through stem cuttings is a popular method world-wide for species such as fruit tree rootstocks and forest trees. Adventitious root (AR) formation from stem cuttings is crucial for effective and successful clonal propagation of apple rootstocks. Strigolactones (SLs) are newly identified hormones, involved in AR formation. However, the regulatory mechanisms underpinning this process remain elusive. In this study, weighted gene co-expression network analysis (WGCNA), and rooting assays using stable transgenic apple materials, revealed that MdBRC1 served as a key gene in the inhibition of AR formation by SLs. We have demonstrated that MdSMXL7 and MdWRKY6 synergistically regulated MdBRC1 expression, depending on the interactions of MdSMXL7 and MdWRKY6 at the protein level downstream of SLs as well as the direct promoter binding on MdBRC1 by MdWRKY6. Furthermore, biochemical studies and genetic analysis revealed that MdBRC1 inhibited AR formation by triggering the expression of MdGH3.1 in a transcriptional activation pathway. Finally, our study not only proposes a novel component, MdWRKY6, that enables MdSMXL7 to regulate MdBRC1 during the process of SLs-controlled AR formation in apple, but also provides prospective target genes to enhance AR formation capacity using CRISPR technology, particularly in woody plants.