High-impact genetic variants associated with neurodevelopmental disorders provide biologically defined entry points for etiological discovery. The 3q29 deletion (3q29Del) is one such variant that confers a ~40-fold increased risk for schizophrenia, and a ~30-fold increased risk for autism. However, the specific neural mechanisms underlying this link remain largely unknown. Here, we report the first in vivo quantitative neuroimaging study in 3q29Del subjects (N = 24) and healthy controls (N = 1,608) using structural MRI. Given prior reports of posterior fossa abnormalities in 3q29Del, we focus our investigation on the cerebellum and its primary tissue-types. Additionally, we compare the prevalence of cystic/cyst-like malformations of the posterior fossa between 3q29Del subjects and controls, and examine the association between neuroanatomical findings and standardized behavioral measures to probe gene-brain-behavior relationships. 3q29Del subjects had smaller cerebellar cortex volumes than controls, both before and after correction for intracranial volume (ICV). 3q29Del subjects also had larger cerebellar white matter volumes than controls following ICV-correction. The 3q29Del group displayed an elevated rate of posterior fossa arachnoid cysts and mega cisterna magna findings independent of cerebellar volume. Sex played a moderating role in a subset of findings. Cerebellar white matter volume was positively associated with visual-motor integration skills and cognitive ability, while cystic/cyst-like malformations yielded no behavioral link. Abnormal development of posterior fossa structures may represent neuroimaging-based biomarkers in 3q29Del. Results reveal cerebellar associations with sensorimotor and cognitive deficits in 3q29Del and present a novel point of genetic convergence with cerebellar pathology reported in idiopathic forms of neurodevelopmental disease.