Functional magnetic resonance imaging (fMRI) studies in conduct disorder and in oppositional defiant disorder have shown inconsistencies. The aim of this meta-analysis of fMRI studies in disruptive behavior disorders was to establish the most consistent brain dysfunctions and to address task- and subtype-related heterogeneity. Web-based publication databases were searched to conduct a meta-analysis of all whole-brain fMRI studies of youths with disruptive behavior disorder or conduct problems up to August 2015. Sub-meta-analyses were conducted in functional subdomains of emotion processing; in cool and hot executive functions, which refer to goal-directed higher cognitive functions with and without motivational and affective significance; and in a subgroup of youths with additional psychopathic traits. The authors performed a meta-analysis of voxel-based group differences in functional activation using the anisotropic effect-size version of seed-based d mapping. Across 24 studies, 338 youths with disruptive behavior disorder or conduct problems relative to 298 typically developing youths had consistent underactivation in the rostral and dorsal anterior cingulate and in the medial prefrontal cortex and ventral caudate. Sub-meta-analyses of fMRI studies showed that medial fronto-cingulate dysfunction was driven by hot executive function. The sub-meta-analysis of emotion processing fMRI studies showed the most consistent underactivation in the dorsolateral prefrontal cortex and temporal pole, while cool executive functions were associated with temporal abnormalities. Youths with disruptive behavior disorder with psychopathic traits showed reduced ventromedial prefrontal-hypothalamic-limbic activation, but they also showed hyperactivation in cognitive control mediating dorsolateral prefrontal-dorsal and striatal regions. The findings show that the most consistent dysfunction in youths with disruptive behavior disorder is in the rostro-dorsomedial, fronto-cingulate, and ventral-striatal regions that mediate reward-based decision making, which is typically compromised in the disorder. Youths with psychopathic traits, on the other hand, have dysfunctions associated with the ventromedial prefrontal cortex and limbic system, together with dorsal and fronto-striatal hyperfunctioning, which may reflect poor affect reactivity and empathy in the presence of hyperactive executive control. These findings provide potential targets for neurotherapeutic and pharmacological interventions.