Plants continuously respond to changing environmental conditions to prevent damage and maintain optimal performance. To regulate gas exchange with the environment and to control abiotic stress relief, plants have pores in their leaf epidermis, called stomata 1. Multiple environmental signals affect the opening and closing of these stomata 2. Heat promotes stomatal opening (to cool down) and drought induces stomatal closing (to prevent water loss). Coinciding stress conditions, however, may evoke conflicting stomatal responses, but the cellular mechanisms to resolve these conflicts are unknown. Here, we demonstrate that the high temperature-associated kinase TARGET OF TEMPERATURE 3 (TOT3) directly controls the activity of plasma membrane H+-ATPases to induce stomatal opening. This TOT3 activity is directly antagonized by OPEN STOMATA 1 (OST1), to prevent water loss during drought stress. This signaling axis harmonizes conflicting heat and drought signals to regulate stomatal aperture. In the context of global climate change, understanding how conflicting stress signals converge on stomatal regulation allows the development of climate change-ready crops.