Plants emit diverse volatile organic compounds (VOCs) from their leaves and roots for protection against biotic and abiotic stress. An important signaling cascade activated by aboveground herbivory is the jasmonic acid (JA) pathway that stimulates the production of VOCs. So far it remains unclear if the activation of this pathway also leads to enhanced VOC emissions from conifer roots, and how the interplay of above- and belowground defenses in plants are affected by multiple stressors. Therefore, we simultaneously analyzed needle and root VOC emissions of Picea abies saplings, as well as CO2 and H2O fluxes in response to aboveground JA treatment, heat stress and their interaction in a controlled climate chamber experiment. Continuous online VOC measurements by PTR-TOF-MS showed an inverse pattern of total needle and root VOC emissions, when plants were treated with JA and heat. While needle sesquiterpene emissions increased nine-fold one day after JA application, total root VOC emissions decreased. This was mainly due to reduced emissions of acetone and monoterpenes by roots. In response to aboveground JA treatment, root total carbon emitted as VOCs decreased from 31% to only 4%. While VOC emissions aboveground increased, net CO2 assimilation strongly declined due to JA treatment, resulting in net respiration during the day. Interestingly, root respiration was not affected by aboveground JA application. Under heat the effect of JA on VOC emissions of needles and roots was less pronounced. The buffering effect of heat on VOC emissions following JA treatment points towards an impaired defense reaction of the plants under multiple stress. Our results indicate efficient resource allocation within the plant to protect threatened tissues by a rather local VOC release. Roots may only be affected indirectly by reduced belowground carbon allocation, but are not involved directly in the JA-induced stress response.