Temperature is one of the most impactful environmental factors in response to which plants adjust their growth and development. While the regulation of temperature signaling has been extensively investigated for the aerial part of plants, much less is known and understood about how roots sense and modulate their growth in response to fluctuating temperatures. Here we found that shoot and root growth responses to high ambient temperature are negatively correlated during early seedling development. A shoot signaling module that includes HY5, the phytochromes and the PIFs exerts a central function in coupling these responses and triggers long-distance signaling to control root growth and auxin levels in the root. In addition to the HY5/PIF dependent shoot module, a local regulatory axis composed of auxin biosynthesis and auxin perception factors mediates root responses to high ambient temperature. Together, our findings uncover that roots integrate long-distance signals with local hormonal inputs during thermomorphogenesis. Overall design: Analysis of short-term (4hours) response to higher ambient temperature in wild type, hy5 and phyAB plants