ABSTRACT Background Apathy is the most prevalent and characteristic neuropsychiatric feature of Huntington's disease. Congruent with the main early pathological changes, apathy is primarily associated with subcortical damage in frontal‐striatal circuits. However, little is known about its precise subserving mechanisms and the contribution of regions other than the basal ganglia. Objectives We aimed to define the neural correlates of apathy in Huntington's disease based on gray matter volume and PET/CT of 18F‐fluorodeoxyglucose metabolism. Methods We rated the severity of apathy in 40 mild Huntington's disease participants using the Problem Behaviors Assessment for Huntington's disease. Voxelwise regression analysis was performed, controlling for effects of potential confounders, and PET/CT results were corrected for the effects of gray matter atrophy. Results Apathy was strongly associated with decreased gray matter within a spatially distributed cortico‐subcortical network, with major compromise of the bilateral amygdala and temporal cortex. PET metabolism was significantly decreased in frontotemporal and parietal regions. Metabolic uptake and gray matter values in the identified clusters showed significant correlations with multiple clinical measures. Conclusions Our findings indicate that apathy in Huntington's disease is not exclusively a consequence of basal ganglia and related frontal‐executive alterations. It is subserved by a complex cortico‐subcortical network where critical reward and emotional‐related prefrontal, temporal, and limbic nodes contribute strongly to its severity. This highlights the contribution of damage in regions other than the basal ganglia to the clinical expression of Huntington's disease. © 2018 International Parkinson and Movement Disorder Society