Domestication converts perennial and photoperiodic ancestral cotton to day-neutral cotton varieties, and the selection of short-season cotton varieties is one of the major objectives of cotton breeding. However, little is known about the mechanism of flowering time in cotton. Here, we report a cotton HD-ZIP I-class transcription factor (GhHB12) specifically expressed in axillary buds, which antagonisticlly interacts with GhSPL10/13 to repress the expression of GhFT, GhFUL, and GhSOC1, resulting in bushy architecture and delayed flowering under long-day conditions. We found that GhHB12-mediated ancestral upland cotton phenotypes (bushy architecture and delayed flowering) could be rescued under short-day conditions. We showed that overexpressing of GhrSPL10 partially rescues the bushy architecture and delayed flowering phenotypes, while overexpression of GhmiR157 reinforced these phenotypes in GhHB12-overexpressing plants. This study defines a regulatory module which regulates cotton architecture, phase transition and could be applied in the breeding of early maturing cotton varieties.