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Although learning and adapting to visuo-motor tasks is critical to child development and health conditions requiring rehabilitation, the neural processes involved in learning a new visuo-motor task and adapting it to novel conditions such as execution with an untrained limb are not fully understood. Therefore, we trained 27 healthy, right-hand-dominant individuals aged 18–35 years to perform a multidirectional point-to-point visually rotated aiming task with a joystick during functional magnetic resonance imaging, with 13 participants learning the task with the dominant (D) and 14 with the non-dominant (ND) hand. All individuals performed the task with the trained and untrained hand before and after training. As expected, performance of both the trained and the untrained hand improved significantly over the course of task acquisition. Brain functional changes associated with adaptation to the demands of the task, and execution differed significantly between D and ND groups. In particular, the ND group showed greater recruitment of visual and motor regions (left middle occipital and left precentral gyri) than the D group during task acquisition. In addition, the D group exhibited greater recruitment of motor planning regions (left precuneus) that contribute to performance with the trained hand, even after bilateral transfer—switching from the trained to non-trained hand. The D group showed more persistence of activation in sensorimotor regions—greater activation when returning to the rotated task after a switching to a simpler, non-rotated aiming task for a short interval. Finally, the D group showed more activation after-effects—increases in simpler task activation after training on the visually rotated task. The findings suggest that brain functional changes associated with adaptation to a visuo-motor skill may differ substantially depending on whether the dominant or non-dominant hand is trained, with non-dominant-hand training associated with greater activation during acquisition, and dominant-hand training associated with greater activation during bilateral transfer, persistence, and after-effects. [ABSTRACT FROM AUTHOR]