DPB1 and DPA1 genes share the same promoter region. Single-nucleotide polymorphisms (SNPs) within the regulatory regions of DP have been reported. This study hypothesizes that by including the SNPs in the promoter region of DP, extended haplotypes are defined, and promoter polymorphism is more extensive than what is currently reported. To identify the SNPs in the region of interest, the DP region spanning 21.5 kb was amplified in three separate long-ranged polymerase chain reactions. A DNA panel consisting of 100 samples was selected to represent a broad range of DPB1 alleles. The panel was amplified and sequenced using a dual sequencing strategy. Binary alignment map (BAM) alignments were generated and the mapped sequence alignments were analyzed using Integrative Genomics Viewer. A total of 76 SNPs were identified, and SNPs were clustered into 12 SNP-linked haplotypes. Multiple sequence alignments of promoter sequences indicated four distinct lineages within the connective region (CR) between two genes. The relationship between DPA1, CR, DPB1, and amino acid motifs was found to be correlated with HV1 and HV6. Of the 12 promoter haplotypes, DPB1 alleles observed with ProDP-4 were in complete linkage with HV1/2/5/6, the rs9277534G SNP, and the highly immunogenic T-cell epitope group. Multiple extended haplotypes of different intronic subtypes of the same DPB1 alleles were also identified. This new view of the full DP haplotype shows the relation of polymorphism, genes, and alleles, and provides a basis for future functionality related nomenclature. The novel clustering of the DP-extended haplotype warrants future investigations of DP haplotype matching in the outcome of haematopoietic stem cell transplantation (HSCT).