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Interspecific breeding in cotton takes advantage of genetic recombination among desirable genes from different parental lines. However, the expression new alleles (ENAs) from crossovers within genic regions and their significance in fibre length (FL) improvement are currently not understood. Here, we generated resequencing genomes of 191 interspecific backcross inbred lines derived from CRI36 (Gossypium hirsutum) × Hai7124 (Gossypium barbadense) and 277 dynamic fibre transcriptomes to identify the ENAs and extremely expressed genes (eGenes) potentially influencing FL, and uncovered the dynamic regulatory network of fibre elongation. Of 35 420 eGenes in developing fibres, 10 366 ENAs were identified and preferentially distributed in chromosomes subtelomeric regions. In total, 1056-1255 ENAs showed transgressive expression in fibres at 5-15 dpa (days post-anthesis) of some BILs, 520 of which were located in FL-quantitative trait locus (QTLs) and GhFLA9 (recombination allele) was identified with a larger effect for FL than GhFLA9 of CRI36 allele. Using ENAs as a type of markers, we identified three novel FL-QTLs. Additionally, 456 extremely eGenes were identified that were preferentially distributed in recombination hotspots. Importantly, 34 of them were significantly associated with FL. Gene expression quantitative trait locus analysis identified 1286, 1089 and 1059 eGenes that were colocalized with the FL trait at 5, 10 and 15 dpa, respectively. Finally, we verified the Ghir_D10G011050 gene linked to fibre elongation by the CRISPR-cas9 system. This study provides the first glimpse into the occurrence, distribution and expression of the developing fibres genes (especially ENAs) in an introgression population, and their possible biological significance in FL.