The ability to carry out two tasks simultaneously, dual tasking, is specifically impaired after traumatic brain injury (TBI). The aim of the present study was to investigate the neuronal correlates to this increased dual cost in chronic severe TBI patients (n = 10) compared to healthy controls (n = 11) using functional magnetic resonance imaging (fMRI) at 3 Tesla (T). The tasks were a visual search and a simple two-fingers button press motor task. Performance data demonstrated similar and significant dual task interference in both TBI patients and controls using a linear mixed model. However, principal component analysis showed that TBI patients and controls could be classified into different categories based on motor activity in the single compared to the dual task condition, thus reflecting the increased variability in the performance in the TBI group. Random effects between-group analysis demonstrated significantly reduced activation in the TBI group in both single task conditions in the occipital and posterior cingulate cortices, and for the visual task also in the thalami. This pattern was reversed in the dual task condition with significantly increased activation of a predominantly left lateralized prefrontal-anterior midline-parietal network in the TBI group compared to the controls. The increase in activation occurred within regions described to be engaged in healthy volunteers as dual task cost increases. This finding points to substitution, functional reorganization within the primary network subserving the task, following TBI, and demonstrates more effortful processing. Recruitment of these additional prefrontal resources may be connected to serial rather than parallel processing in low level dual tasking in TBI. Thus, in severe TBI, low level dual task performance depends on increased attentional and executive guidance.