Upland cotton (Gossypium hirsutum) accounts for more than 90% of the world’s cotton production and, as an allotetraploid, is a model plant for polyploid crop domestication. In the present study, we reported a complete telomere-to-telomere (T2T) genome assembly of Upland cotton accession Texas Marker-1 (T2T-TM-1), which has a total size of 2,299.6 Mb, and annotated 79,642 genes. Based on T2T-TM-1, interspecific centromere divergence was detected between the A- and D-subgenomes and their corresponding diploid progenitors. Centromere-associated repetitive sequences (CRCs) were found to be enriched for Gypsy-like retroelements. Centromere size expansion, repositioning and structure variations occurred post-polyploidization. It is interesting that CRC homologs were transferred from the diploid D-genome progenitor to the D-subgenome, invaded the A-subgenome and then underwent post-tetraploidization proliferation. This suggests an evolutionary advantage for the CRCs of the D-genome progenitor, presents a D-genome-adopted inheritance of centromere repeats after polyploidization and shapes the dynamic centromeric landscape during polyploidization in polyploid species.