Although there are a number of functional neuroimaging studies that have investigated self-initiated and externally-triggered movements, data directly comparing right and left hands in this context are very scarce. The goal of this study was to further understand the role of the basal ganglia and prefrontal cortex in the realm of self-initiated and externally-triggered right and left hand movements. Young healthy right-handed adults performed random, follow and repeat conditions of a finger moving task with their right and left hands, while being scanned with functional magnetic resonance imaging. Significant activation of the dorsolateral prefrontal cortex was observed when comparing the self-initiated movements with the repeated control and externally-triggered movements when using either hand in agreement with its role in monitoring. The caudate nucleus activation was found during self-initiated conditions compared with the control condition when either hand was used, showing that it is particularly involved when a new movement needs to be planned. Significant putamen activation was observed in all within-hand contrasts except for the externally-triggered vs. control condition when using the left hand. Furthermore, greater putaminal activation was found for the left vs. the right hand during the control condition, but for the right vs. the left hand subtraction for the self-initiated condition. Our results show that the putamen is particularly involved in the execution of non-routine movements, especially if those are self-initiated. Furthermore, we propose that, for right-handed people performing fine movements, as far as putamen involvement is concerned, the lack of proficiency of the non-dominant hand may prevail over other task demands.