Broomcorn millet ( L.) is one of the earliest domesticated crops in the world. Weedy broomcorn millet [ (Kitag.) Chang or subsp. (Kitag.) Tzvel] is thought to be the descendant of the wild ancestor or the feral type of this cereal. The genealogical relationships and genetic divergence among these taxa have not been clarified. In this study, the genetic diversity and population structure of weedy and cultivated broomcorn millets were investigated by using the high-throughput sequencing technology, i.e., the specific-locus amplified fragment sequencing (SLAF-seq). Our analyses consistently revealed both the wild and the feral genotypes in the weedy broomcorn millets. The single nucleotide polymorphisms (SNPs) at the genomic level provided useful evidence to distinguish the wild and the endoferal/exoferal types of weedy broomcorn millets. The genetic divergence revealed between the cultivated broomcorn millet from eastern Eurasia and those from central-western Eurasia was probably derived from either the genetic introgression from weedy broomcorn millets along the spread routes or the founder effect, while the limited gene flow of broomcorn millets from eastern and central-western Eurasia was probably due to the different uses of broomcorn millets and eating habits of the local people.