Impaired working memory is a common and disabling consequence of traumatic brain injury (TBI) that is caused by aberrant brain processing. However, little is known about the extent to which deficits are perpetuated by specific working memory subprocesses. Using a combined functional magnetic resonance imaging (fMRI) and working memory paradigm, we tested the hypothesis that the pattern of brain activation subserving working memory following TBI would interact with both task demands and specific working memory subcomponents: encoding, maintenance, and retrieval. Forty-three patients with moderate-severe TBI, of whom 25 were in the acute phase of recovery (M = 2.16 months, SD = 1.48 months, range = 0.69 – 6.64 months) and 18 in the chronic phase of recovery (M = 23.44 months, SD = 6.76 months, range = 13.35 – 34.82 months), were compared with 38 demographically similar healthy controls. Behaviourally, we found that working memory deficits were confined to the high cognitive load trials in both acute (P = 0.006) and chronic (P = 0.024) cohorts. Furthermore, results for a subset of the sample (18 chronic TBI and 17 healthy controls) who underwent fMRI revealed that the TBI group showed reduced brain activation when simply averaged across all task trials (regardless of cognitive load or subcomponent). However, interrogation of the subcomponents of working memory revealed a more nuanced pattern of activation. When examined more closely, patterns of brain activity following TBI were found to interact with both task demands and the working memory subcomponent: increased activation was observed during encoding in the left inferior occipital gyrus whereas decreased activation was apparent during maintenance in the bilateral cerebellum and left calcarine sulcus. Taken together, findings indicate an inability to appropriately modulate brain activity according to task demand that is specific to working memory encoding and maintenance.