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Summary Drought stress substantially impacts crop physiology resulting in alteration of growth and productivity. Understanding the genetic and molecular crosstalk between stress responses and agronomically important traits such as fibre yield is particularly complicated in the allopolyploid species, upland cotton (Gossypium hirsutum), due to reduced sequence variability between A and D subgenomes. To better understand how drought stress impacts yield, the transcriptomes of 22 genetically and phenotypically diverse upland cotton accessions grown under well‐watered and water‐limited conditions in the Arizona low desert were sequenced. Gene co‐expression analyses were performed, uncovering a group of stress response genes, in particular transcription factors GhDREB2A‐A and GhHSFA6B‐D, associated with improved yield under water‐limited conditions in an ABA‐independent manner. DNA affinity purification sequencing (DAP‐seq), as well as public cistrome data from Arabidopsis, were used to identify targets of these two TFs. Among these targets were two lint yield‐associated genes previously identified through genome‐wide association studies (GWAS)‐based approaches,GhABP‐DandGhIPS1‐A. Biochemical and phylogenetic approaches were used to determine thatGhIPS1‐Ais positively regulated by GhHSFA6B‐D, and that this regulatory mechanism is specific toGossypiumspp. containing the A (old world) genome. Finally, an SNP was identified within the GhHSFA6B‐D binding site inGhIPS1‐Athat is positively associated with yield under water‐limiting conditions. These data lay out a regulatory connection between abiotic stress and fibre yield in cotton that appears conserved in other systems such as Arabidopsis.