The genetic gain in wheat production has slowed over the last couple decades due to the draining of the gene pool usable in wheat breeding. The limited genetic variability of the wheat genome has increasingly become a bottleneck for wheat improvement. There is a constant need to find and deploy new relevant genes in wheat to sustain and improve wheat productivity under emerging biotic and abiotic stresses. The polyploid origin of the wheat genome had omitted tremendous genetic variation, leading to a narrow genetic base in wheat. Those evolutionarily-lost genetic variation mostly remains in the ancestors and relatives of wheat and can be artificially brought back to wheat by homoeologous recombination-based chromosome engineering (HRBCE). Recent advances in wheat genomics, especially high-throughput genotyping and reference genome sequences, have provided great potential to improve the efficacy and throughput of HRBCE in harnessing the genetic diversity of wild species for wheat improvement and in the genome studies as well. Here we report our research progress toward the diversification and understanding of the wheat B genome, whose ancestor remains obscure, by genomics-enabled HRBCE and comparative genome analysis. We have incorporated the genes for resistance to rusts, Fusarium head blight, tan spot, and Septoria nodorum blotch, and those for tolerance to salt and waterlogging from Aegilops speltoides (2n = 2x = 14, SS) and Thinopyrum elongatum (2n = 2x = 14, EE) into the wheat B genome and produced over one thousand B-S and B-E recombinants by ph1b-induced homoeologous recombination. This has enriched the wheat B genome and extended its genetic variability. In addition, we have constructed composite bin maps of the B-genome chromosomes based on B-S and B-E recombination and wheat 90K SNP assay, and developed a unique physical framework useful for further study of the B genome and its potential donors. Meanwhile, we determined the nucleotide position of the ph1b deletion and developed ph1b-specific DNA markers, which were not available before. They are extremely useful in ph1b-mediated gene introgression and genome study. Moreover, we revealed new insight into the involvement of Ae. speltoides in the origin of the wheat B genome by comparative genome analysis and concluded that the B genome might have a polyphyletic origin with multiple ancestors involved, including Ae. speltoides. In summary, HRBCE enriches and diversifies the wheat genome, and facilitates genome studies in wheat and its relatives especially in the genomics era.