The dual-action simulation hypothesis proposes that both an observed and an imagined action can be represented simultaneously in the observer’s brain. These two sensorimotor streams would either merge or compete depending on their relative suitability for action planning. To test this hypothesis, three forms of combined action observation and motor imagery (AO+MI) instructions were used in this repeated-measures experiment. Participants observed index finger abduction-adduction movements while imagining the same action (congruent AO+MI), little finger abduction-adduction (coordinative AO+MI), or a static hand (conflicting AO+MI). Single-pulse transcranial magnetic stimulation was applied to the left primary motor cortex. The amplitude of motor evoked potential responses were recorded from both the first dorsal interosseous (FDI) and abductor digiti minimi (ADM) muscles of the right-hand while eye movements were tracked. When controlling for the influence of relevant eye movements, corticospinal excitability was facilitated relative to control conditions in the concurrently observed and imagined muscles for both congruent and coordinative AO+MI conditions. Eye-movement metrics and social validation data from post-experiment interviews provided insight into the cognitive mechanisms underlying these effects. The findings provide empirical support for the dual-action simulation hypothesis, indicating for the first time that it is possible to co-represent observed and imagined actions simultaneously.