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Bacterial blight (BB) in cotton (Gossypium hirsutum L.) is caused by the gram‐negative bacterium Xanthomonas citri pv. malvacearum (Xcm), and Xcm Race 18 is the most prevalent and virulent bacterium across the U.S. Cotton Belt. The objectives of this study were to investigate the genetic basis of resistance to Xcm Race 18 in U.S. upland cotton (Gossypium hirsutum) as broadly represented by 34 resistant obsolete U.S. upland accessions and 29 resistant commercial cultivars and elite breeding lines spanning a century of breeding efforts. Segregation in resistance was analyzed in F2 populations from crosses between the resistant parents and one or two susceptible parents (one upland: Acala Ultima or NM 14T1330, and one G. barbadense: NMSI E2032). A total of 111 F1, 95 F2, and 23 F2:3 populations were artificially inoculated with Xcm Race 18 to investigate segregation ratios for BB resistance. All F1 were resistant, and 65 F2 populations derived from 52 resistant parents exhibited the expected 3:1 resistant/susceptible ratio for resistance to Xcm Race 18, indicating a dominant resistance gene conferring the resistance. The analysis of DNA markers that are tightly linked to the B12 gene on chromosome c14 (D02) showed that all the resistant germplasms tested possessed the B12 gene and they were co‐segregating with BB resistance, indicating that the B12 locus is broadly distributed within the U.S. upland cotton. The results point to the need to discern if these resistant lines carry different B12 alleles or different but tightly linked resistance loci including B12.