Attention-deficit/hyperactivity disorder (ADHD) is associated with cognitive performance and functional brain changes that are sensitive to task conditions, indicating a role for dynamic impairments rather than stable cognitive deficits. Prominent hypotheses consistent with this observation are a failure to optimise brain arousal or activation states. Here we investigate cortical activation during different conditions. Using a sample of 41 non-comorbid adults with ADHD and 48 controls, we examine quantitative EEG activity during a resting state, a cued continuous performance test with flankers (CPT-OX) and the sustained attention to response task (SART). We further investigate the effects of methylphenidate in a subsample of 21 ADHD cases. Control participants showed a task-related increase in theta activity when engaged in cognitive tasks, primarily in frontal and parietal regions, which was absent in participants with ADHD. Treatment with methylphenidate resulted in normalisation of the resting state to task activation pattern. These findings suggest that ADHD in adults is associated with insufficient allocation of neuronal resources required for normal cortical activation commensurate with task demands. Further work is required to clarify the causal role of the deficit in cortical activation and provide a clearer understanding of the mechanisms involved.