The prefrontal cortex is essential for exerting top-down control over posterior regions. However, its underlying long-range connectivity patterns remain poorly understood. Neuroimaging evidence suggests that the frontal eye field (FEF) and the inferior frontal junction (IFJ) are specialized in the control of spatial vs non-spatial processing, respectively. We hypothesized that their specialization may be supported by their connectivity fingerprints. We investigated the multimodal connectomes of the FEF and IFJ by leveraging the results of an activation likelihood estimation (ALE) fMRI meta-analysis. Each region’s ALE peak coordinate was used as a seed to perform a meta-analytic connectivity modeling (MACM) analysis to uncover their whole-brain coactivation patterns. We then performed a reverse inference on the ensuing brain networks to characterize their associations with specific behavioral domains. Crucially, the same seeds were used for surface-based probabilistic tractography using 3T diffusion MRI data from the Human Connectome Project. We tracked streamlines to the dorsal and ventral visual streams on each subject's native surface parcellated using the Glasser atlas. MACM showed that the FEF coactivates with the IFJ, the superior/inferior parietal lobule and the supplementary/cingulate eye fields, whereas the IFJ additionally coactivates with the insular and inferotemporal cortices. The IFJ coactivations were associated with a wider spectrum of behavioral domains compared to FEF. Using surface-based tractography, we found predominant structural connectivity from the left FEF to the dorsal visual stream, and from the bilateral IFJ to the ventral visual stream. These results cannot be explained by seed-to-target distance. We also evaluated the influence of the parcellation scheme (Glasser, Schaefer) and the surface seeding strategy by performing bidirectional tracking. The connectivity fingerprints of FEF and IFJ provide converging evidence of their functional specialization. From a network perspective, these results highlight that the two visual stream architecture extends into the prefrontal cortex, consistent with non-human primate evidence.