This study examined whether disruptions in connectivity involving regions critical for learning, planning, and executing movements are relevant to core autism symptoms. Spatially constrained ICA was performed using resting-state fMRI from 419 children (autism spectrum disorder (ASD) = 105; typically developing (TD) = 314) to identify functional motor subdivisions. Comparing the spatial organization of each subdivision between groups, we found voxels that contributed significantly less to the right posterior cerebellar component in children with ASD versus TD (P <0.001). Next, we examined the effect of diagnosis on right posterior cerebellar connectivity with all other motor subdivisions. The model was significant (P = 0.014) revealing that right posterior cerebellar connectivity with bilateral dorsomedial primary motor cortex was, on average, stronger in children with ASD, while right posterior cerebellar connectivity with left-inferior parietal lobule (IPL), bilateral dorsolateral premotor cortex, and supplementary motor area was stronger in TD children (all P ≤0.02). We observed a diagnosis-by-connectivity interaction such that for children with ASD, elevated social-communicative and excessive repetitive-behavior symptom severity were both associated with right posterior cerebellar-left-IPL hypoconnectivity (P ≤0.001). Right posterior cerebellar and left-IPL are strongly implicated in visuomotor processing with dysfunction in this circuit possibly leading to anomalous development of skills, such as motor imitation, that are crucial for effective social-communication. LAY SUMMARY: This study examines whether communication between various brain regions involved in the control of movement are disrupted in children with autism spectrum disorder (ASD). We show communication between the right posterior cerebellum and left IPL, a circuit important for efficient visual-motor integration, is disrupted in children with ASD and associated with the severity of ASD symptoms. These results may explain observations of visual-motor integration impairments in children with ASD that are associated with ASD symptom severity.