"Slips of action" occur in everyday life when we momentarily lose sight of a goal (for example, when in a rush or distracted). Associative models propose that these habitual responses can be activated via a direct stimulus-response (S-R) mechanism, regardless of the current hedonic value of the outcome. The slips-of-action task (SOAT) has been extensively used in both healthy and pathological populations to measure habit tendencies, the likelihood of making erroneous responses for devalued outcomes. Inspection of behavioral performance does not reveal, however, whether the impairments were due to impaired goal-directed control or aberrantly strong habit formation. In the current study, we used functional MRI while human participants performed both the instrumental training and SOAT test phases, to elucidate the relative contributions of these mechanisms to performance on the SOAT. On trials in which conflict arises between competing goal-directed and habitual responses, we observed increased activation across areas including the anterior cingulate cortex, paracingulate gyrus, lateral orbitofrontal cortex (OFC), insula, and inferior frontal gyrus (IFG). Responding for devalued outcomes was related to increased activation in the premotor cortex and cerebellum, implicating these regions in habitual responding. Increased activation in the caudate, dorsolateral prefrontal cortex (dlPFC), and frontal pole during training was associated with better performance during the test phase, indicative of goal-directed action control. These results endorse interpretation of the SOAT in terms of competing goal-directed and habitual mechanisms and highlight that cognitive control processes present an additional bottleneck for successful performance on this task.