Previous studies have reported that multiple brain regions are activated during spatial navigation, but it remains unclear how this activation is converted to motor commands for navigation. This study was aimed to investigate synchronization across different brain regions and between cortical areas and muscles during spatial navigation. This synchronization has been suggested to be essential for integrating activity in the multiple brain areas to support higher cognitive functions and for conversion of cortical activity to motor commands. In the present study, the subjects were required to sequentially trace ten checkpoints in a virtual town by manipulating a joystick and to perform this three times while electroencephalograms and electromyograms from the right arm were monitored. Time spent on the task in the third trial was significantly lesser than that in the first trial indicating an improvement in task performance. This repeated learning was associated with an increase in alpha power at the electrodes over the contralateral sensorimotor region and in theta power at the electrodes over the bilateral premotor and frontotemporal regions. Alpha- and theta-range corticocortical coherences between these regions and other brain areas were also increased in the third trial compared to the first trial. Furthermore, alpha- and theta-range corticomuscular coherence was significantly increased in the second and third trials compared to the first trial. These results suggest that alpha- and theta-range synchronous activity across multiple systems is essential for the integrated brain activity required in spatial navigation and for the conversion of this activity to motor commands.