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The United States Department of Agriculture, Soybean Germplasm Collection includes 18,480 domesticated soybean and 1,168 wild soybean accessions introduced from 84 countries or developed in the U.S. This collection was genotyped with the SoySNP50K BeadChip containing greater than 50K SNPs. Redundant accessions were identified in the collection and distinct genetic backgrounds of soybean from different geographic origins were observed that could be a unique resource for soybean genetic improvement. We detected a dramatic reduction of genetic diversity based on linkage disequilibrium and haplotype structure analyses of the wild, landrace and North American cultivar populations and identified candidate regions associated with domestication and selection imposed by North American breeding. We constructed the first soybean haplotype block maps in the wild, landrace and North American cultivar populations and observed that most recombination events occurred in the regions between haplotype blocks. These haplotype maps are crucial for association mapping aimed at the identification of genes controlling traits of economic importance. A case-control association test delimited potential genomic regions along seven chromosomes that most likely contain genes controlling seed weight in domesticated soybean. The resulting dataset will facilitate germplasm utilization, identification of genes controlling important traits, and will accelerate the creation of soybean varieties with improved seed yield and quality.