Neuroimaging studies suggest that changes in the cerebellar-basal ganglia-thalamo-cortical sensorimotor circuit are a pathophysiologic feature of focal dystonia. However, it remains unclear whether structural and functional alterations vary in different forms of focal dystonia. Thus, in patients with cervical dystonia (CD) and blepharospasm (BSP), we aimed to investigate structural damage and resting-state functional alterations using whole-brain and seed-based approaches to test the hypothesis of possible functional connectivity (FC) alterations in specific circuits, including the cerebellum, basal ganglia, and cerebral cortex, in the context of preserved global FC. In this cross-sectional study, we applied a multimodal 3T MRI protocol, including 3-dimensional T1-weighted images to extract brain volumes and cortical thickness, and fMRI at rest to study FC of the dentate nucleus and globus pallidus with a seed-based approach and whole-brain FC with a graph theory approach. This study included 33 patients (17 with CD [14 female] age 55.7 ± 10.1 years, 16 with BSP [11 female] age 62.9 ± 8.8 years) and 16 age- and sex-matched healthy controls (HC) (7 female) 54.3 ± 14.3 years if age. Patients with CD, patients with BSP, and HC did not differ in terms of cortical or subcortical volume. Compared to HC, both patients with CD and patients with BSP had a loss of dentate FC anticorrelation with the sensorimotor cortex. Patients with CD and those with BSP showed increased pallidal FC with the cerebellum, supplementary motor area, and prefrontal cortices with respect to HC. Increased dentate FC with the cerebellum and thalamus and increased pallidal FC with the bilateral thalamus, sensorimotor and temporo-occipital cortices, and right putamen were present in patients with CD but not patients with BSP compared to HC. Measures of global FC, that is, global efficiency and small-worldness, did not differ between patients and HC. Both patients with CD and those with BSP showed altered dentate and pallidal FC with regions belonging to the integrated cerebellar-basal ganglia-thalamo-cortical sensorimotor circuit, supporting the concept that focal dystonia is a disorder of specific networks and not merely a result of basal ganglia alterations in the context of a preserved whole-brain functional architecture. Differences in functional interplay among specific brain structures may distinguish CD and BSP.