Navigated transcranial magnetic stimulation (TMS) in combination with electromyography (EMG) recordings can be used to map the brain regions in which TMS evokes motor-evoked potentials (MEPs) in certain muscles. Navigated TMS (nTMS) is used increasingly to identify the functional motor area of different muscles for clinical applications, including neurosurgical planning. However, the accuracy of TMS-based mapping of functional motor areas may depend on the TMS-induced current direction due to anisotropic cortical morphology, complicating association of the functional motor maps with neuroanatomical structures. Furthermore, it is not clear how well nTMS can distinguish nearby muscle representations on the cortical surface. We therefore investigated the functional motor maps obtained with posterior-to-anterior (PA) and lateral-to-medial (LM) TMS-induced currents within a spatially defined area by stimulating targets in a grid of locations over the left primary motor cortex in 8 healthy participants. Results were compared to functional MRI (fMRI) activation maps obtained using a voluntary opposing thumb movement task. We found that TMS applied with PA-induced currents identifies a motor area that is located significantly more anterior (8.7 -10.4 mm depending on the muscle) with respect to an MEP motor area identified using LM-induced currents for the same muscle. Motor maps obtained with LM-induced currents show more overlap with the motor map identified using fMRI compared to PA-induced currents. In conclusion, the spatial representation of the MEP motor map identified by TMS is dependent on the direction of the induced current. These findings suggest that the application of nTMS using an LM-induced current direction corresponds best with the hand motor area as measured with fMRI.