The brain’s ability to flexibly chain elementary movements into sequences enables rich behavior. For example, a concert pianist can play a never-before-seen sonata from the sheet music. However, to achieve the fluid and error-free performance required for a concert, she extensively practices a single piece until it is automatic. The neural circuits underlying automatic motor sequences are thought to differ from those for executing flexible ones, but the distinction is poorly understood. To address this, we trained rats to execute sequences of three lever presses in flexible sessions – where cues instructed the sequence order – or automatic ones – where a single uncued sequence was repeated. We found that neural activity in sensorimotor striatum primarily encodes low-level kinematics, regardless of the execution mode or sequence, whereas motor cortex activity reflects higher-level sequence information. Consistent with this, lesions to sensorimotor striatum disrupted movement kinematics in both modes, but only eliminated motor sequence execution in the automatic sessions. Lesions of motor cortex disrupted flexible sequence execution, indicating its vital role in sequencing motor elements. Intriguingly, automatic motor sequences were also affected by motor cortex lesions, unless we trained rats only on the automatic mode in which case performance was largely spared. This suggests that demands for flexibility interfere with subcortical consolidation of automatic motor sequences. We developed a neural network model with cortical and subcortical pathways, where the latter assumes control of behavior as it learns to recapitulate motor cortical commands. Our model reproduces the above findings, and suggests that flexible sequencing interferes with consolidation when the subcortical pathway lacks the sensory inputs needed to differentiate between sequences. This work provides important insights into the hierarchical and distributed control of flexible and automatic motor sequences and characterizes the circumstances under which the motor cortex is essential for sequence execution.