The thalamus is composed of functionally and structurally distinct nuclei. Previous studies have indicated that certain cortical areas may project across multiple thalamic nuclei, potentially allowing them to modulate distributed information flow. However, there is a lack of quantitative investigations into anatomical connectivity patterns within the thalamus. Consequently, it remains unknown if cortical areas exhibit differences in the spread of their thalamic connectivity patterns. To address this knowledge gap, we used diffusion magnetic resonance imaging (dMRI) to compute brain-wide probabilistic tractography using data from 828 healthy adults collected by the Human Connectome Project. To measure the spatial extent of anatomical connectivity patterns within the thalamus, we developed an innovative framework that quantifies the spatial properties of each cortical area’s within-thalamus connectivity patterns. We then leveraged resting-state functional MRI, cortical myelin, and human neural gene expression data to test if the spread of within-thalamus connectivity patterns varied along the cortical hierarchy. These results revealed two broad cortico-thalamic tractography motifs: 1) a sensorimotor cortical motif characterized by focal thalamic connections targeting posterolateral thalamus, which potentially supports fast, feed-forward information flow; and 2) an associative cortical motif characterized by diffuse thalamic connections targeting anteromedial thalamus, which potentially supports slower, feed-back information flow. These results were consistent among human subjects and were also observed in macaques, indicating cross-species generalizability. In summary, these findings demonstrate that sensorimotor and association cortical areas exhibit differences in the spatial extent of their within-thalamus connectivity patterns, which may support functionally-distinct cortico-thalamic information transmission.