During task executions, brain activity increases in executive networks (ENs) and decreases in default-mode networks (DMNs). Here, we examined whether these large-scale network dynamics can be influenced by unconscious cognitive information processing. Volunteers saw instructions (cues) to respond either ipsilaterally or contralaterally to a subsequent lateralized target. Unbeknownst to them, each cue was preceded by a masked stimulus (prime), which could be identical (congruent), or opposite (incongruent) to the cue, or neutral (not an instruction). Behaviorally, incongruent primes interfered with performance, even though they were not consciously perceived. With functional magnetic resonance imaging, we individuated the anticorrelated ENs and DMNs involved during task execution. With effective connectivity analyses, we found that DMNs caused activity in ENs throughout the task. Unconscious interference during incongruent trials was associated with a specific activity increase in ENs and an activity drop in DMNs. Intersubject efficiency in performance during incongruent trials was correlated with functional connectivity between specific ENs and DMNs. These results indicate that unconscious instructions can prime activity in ENs and DMNs and suggest that the DMNs play a key role in unconscious monitoring of the environment in the service of efficient resource allocation for task execution.