Plants respond to diurnal and seasonal changes in temperature by reprogramming vital developmental pathways. Understanding the molecular mechanisms that define environmental modulation of plant growth and reproduction is critical in the context of climate change that threatens crop yield worldwide. Here, we report that elevated temperature accelerates fruit dehiscence in members of the Brassicaceae family including the model plant Arabidopsis thaliana and important crop species. Arabidopsis fruit development is controlled by a network of interacting regulatory genes. Among them, the INDEHISCENT (IND) gene is a key regulator of the valve-margin tissue that mediates fruit opening, hence facilitating fruit dehiscence. We demonstrated that the valve-margin development is accelerated at higher temperature and that IND is targeted for thermosensory control. Our results reveal that IND upregulation is facilitated via temperature-induced chromatin dynamics leading to accelerated valve-margin specification and dispersal of the seed. Specifically, we show that temperature-induced changes in IND expression are associated with thermosensory H2A.Z nucleosome dynamics. These findings establish a molecular framework connecting tissue identity with thermal sensing and set out directions for the production of temperature-resilient crops.