High temperature promotes guard cell expansion, which opens stomatal pores to facilitate leaf cooling. How the high temperature signal is perceived and transmitted to regulate stomatal aperture is, however, unknown. Here, we used a reverse-genetics approach to understand high temperature-mediated stomatal opening in Arabidopsis thaliana. Our findings reveal that high temperature-induced guard cell movement requires components involved in blue light-mediated stomatal opening, suggesting crosstalk between light and temperature signalling pathways. The molecular players involved include phototropin photoreceptors, plasma membrane H+-ATPases, and multiple members of the 14-3-3 protein family. We further show that phototropin-deficient mutants display impaired rosette evapotranspiration and leaf cooling at high temperatures. Blocking the interaction of 14-3-3 proteins with their client proteins severely impairs high temperature-induced stomatal opening, but has no effect on the induction of heat-sensitive guard cell transcripts, supporting the existence of an additional intracellular high-temperature response pathway in plants.