"Converted" left-handers are innately left-handed individuals forced as children to write with the right nondominant hand. We asked how a left-to-right handwriting switch shapes cortical sensorimotor representations of finger movements. In 16 adult converted left-handers and age-matched groups of 16 consistent right-handers and 16 left-handers, we studied movement-related neuronal activity with functional magnetic resonance imaging while participants performed simple unimanual and bimanual movements with right and left index fingers. In converted left-handers, movement-related activity in the primary sensorimotor hand area (SM1) and caudal dorsal premotor cortex (PMd) of the nondominant left hemisphere correlated with the left-to-right shift in handedness. The more right-handed converted left-handers had become, the greater the sensorimotor activation in these areas. Between-group comparisons showed that the switch from left to right hand also reinforced movement representations in the dominant right hemisphere. In converted left-handers, the right inferior parietal cortex and lateral PMd were more active relative to consistent right or left-handers in all motor tasks. These results suggest two distinct neuronal correlates of handedness in human sensorimotor cortex. Although those in executive sensorimotor cortex (i.e., SM1 and adjacent PMd) depend on the hand used throughout life, those in higher-order sensorimotor areas (i.e., inferior parietal cortex and rostrolateral PMd) are invariant and thus cannot be switched to the nondominant hemisphere by educational training.