Predicted increases in atmospheric carbon dioxide (CO2) are widely anticipated to increase biomass accumulation by accelerating rates of photosynthesis in many plant taxa. Little, however, is known about how soil-borne plant antagonists might modify the effects of elevated CO2 (eCO2), with root-feeding insects being particularly understudied. Root damage by insects often reduces rates of photosynthesis by disrupting root function and imposing water deficits. These insects therefore have considerable potential for modifying plant responses to eCO2. We investigated how root damage by a soil-dwelling insect (Xylotrupes gideon australicus) modified the responses of Eucalyptus globulus to eCO2. eCO2 increased plant height when E. globulus were 14 weeks old and continued to do so at an accelerated rate compared to those grown at ambient CO2 (aCO2). Plants exposed to root-damaging insects showed a rapid decline in growth rates thereafter. In eCO2, shoot and root biomass increased by 46 and 35%, respectively, in insect-free plants but these effects were arrested when soil-dwelling insects were present so that plants were the same size as those grown at aCO2. Specific leaf mass increased by 29% under eCO2, but at eCO2 root damage caused it to decline by 16%, similar to values seen in plants at aCO2 without root damage. Leaf C:N ratio increased by >30% at eCO2 as a consequence of declining leaf N concentrations, but this change was also moderated by soil insects. Soil insects also reduced leaf water content by 9% at eCO2, which potentially arose through impaired water uptake by the roots. We hypothesise that this may have impaired photosynthetic activity to the extent that observed plant responses to eCO2 no longer occurred. In conclusion, soil-dwelling insects could modify plant responses to eCO2 predicted by climate change plant growth models.