Networks in the parietal and premotor cortices enable essential human abilities regarding motor processing, including attention and tool use. Even though our knowledge on its topography has steadily increased, a detailed picture of hemisphere-specific integrating pathways is still lacking. With the help of multishell diffusion magnetic resonance imaging, probabilistic tractography, and the Graph Theory Analysis, we investigated connectivity patterns between frontal premotor and posterior parietal brain areas in healthy individuals. With a two-stage node characterization approach, we defined the network role of precisely mapped cortical regions from the Julich-Brain atlas. We found evidence for a third, left-sided, medio-dorsal subpathway in a successively graded dorsal stream, referencing more specialized motor processing on the left. Supplementary motor areas had a strongly lateralized connectivity to either left dorsal or right ventral parietal domains, representing an action-attention dichotomy between hemispheres. The left sulcal parietal regions primarily coupled with areas 44 and 45, mirrored by the inferior frontal junction (IFJ) on the right, a structural lateralization we termed as “Broca’s-IFJ switch.” We were able to deepen knowledge on gyral and sulcal pathways as well as domain-specific contributions in parieto-premotor networks. Our study sheds new light on the complex lateralization of cortical routes for motor activity in the human brain. Author Summary Human motor abilities are processed via specialized yet intertwined pathways in the parietal and premotor cortex. These can be parcellated into networks of brain areas, sharing connection patterns that differ between hemispheres. We differentiated a set of graded pathways, connecting definable network hubs. The well-known Dorsal Stream for visuomotor transformation appears to be left-dominantly divisible into three distinct substreams, providing more anatomical detail about its specialization into visual and semantic segments. Supplementary motor areas show lateralized couplings with left dorsal and right ventral parietal areas, respectively, while left-sided AIPS connectivity to area 44/45 is mirrored by right-sided intersulcal links to the inferior frontal sulcus, both deepening our understanding of incorporated multi-task faculties like attention and speech.