Genome editing provides novel strategies for improving plant traits, but relies on current genetic transformation and plant regeneration procedures, which can be inefficient. We have engineered a barley stripe mosaic virus (BSMV)-based sgRNA delivery vector (BSMV-sg) that is effective in performing heritable genome editing in Cas9-transgenic wheat plants. Mutated progenies were present in the next generation at frequencies ranging from 12.9% to 100% in three different wheat varieties, and 53.8% to 100% of mutants were virus-free. We also achieved multiplex mutagenesis in progeny using a pool of BSMV-sg vectors harboring different sgRNAs. Furthermore, we devised a virus-induced transgene-free editing procedure (VITF-Edit) to generate Cas9-free wheat mutants by crossing BSMV-infected Cas9-transgenic wheat pollen with wild-type wheat. Our study provides a robust, convenient and tissue culture-free approach for genome editing in wheat through virus infection.