Motor system organization varies with handedness. However, previous work has focused almost exclusively on direction of handedness (right or left) as opposed to degree of handedness (strength). In the present study, we determined whether measures of interhemispheric interactions and degree of handedness are related to contra- and ipsilateral motor cortical representations. Participants completed a battery of handedness assessments including both handedness preference measures and behavioral measures of intermanual differences in dexterity, a computerized version of the Poffenberger paradigm (PP) to estimate interhemispheric transfer time (IHTT), and they underwent transcranial magnetic stimulation (TMS) mapping of both motor cortices while we recorded muscle activity from the first dorsal interosseous muscle bilaterally. A greater number of ipsilateral motor evoked potentials (iMEPs) were elicited in less lateralized individuals with the number of iMEPs correlated with IHTT. There were no relationships between handedness or lateralization of dexterity and symmetry of contralateral motor representations, although this symmetry was related to IHTT. Finally, IHTT was positively correlated with multiple measures of laterality and handedness. These findings demonstrate that degree of laterality of dexterity is related to the propensity for exhibiting iMEPs and the speed of interhemispheric interactions. However, it is not clear whether iMEPs are directly mediated via ipsilateral corticospinal projections or are transcallosally transmitted.