Recent studies show that during a simple movement imagery task, the power of sensorimotor rhythms differs according to handedness. However, the effects of motor imagery perspectives on these differences have not been investigated yet. Our study aimed to check how handedness impacts the activity of alpha (8-13 Hz) and beta (15-30 Hz) oscillations during creating a kinesthetic (KMI) or visual-motor (VMI) representation of movement. Forty subjects (20 right-handed and 20 left-handed) who participated in the experiment were tasked with imagining sequential finger movement from a visual or kinesthetic perspective. Both the electroencephalographic (EEG) activity and behavioral correctness of the imagery task performance were measured. After the registration, we used independent component analysis (ICA) on EEG data to localize visual- and motor-related EEG sources of activity shared by both motor imagery conditions. Significant differences were obtained in the visual cortex (the occipital ICs cluster) and the right motor-related area (right parietal ICs cluster). In comparison to right-handers who, regardless of the task, demonstrated the same pattern in the visual area, left-handers obtained higher power in the alpha waves in the VMI task and better performance in this condition. On the other hand, only the right-handed showed different patterns in the alpha waves in the right motor cortex during the KMI condition. The results indicate that left-handers imagine movement differently than right-handers, focusing on visual experience. This provides new empirical evidence on the influence of movement preferences on imagery processes and has possible future implications for research in the area of neurorehabilitation and motor imagery-based brain-computer interfaces (MI-BCIs).