Decoding the genetic profiles underlying the cerebellar functional organization is critical for uncovering the essential role of the human cerebellum in various high-order functions and malfunctions in neuropsychiatric disorders. However, no effort has been made to systemically address this. By combining transcriptome data with the intrinsic functional connectivity of the human cerebellum, we not only identified 443 network-specific genes but also discovered that their gene co-expression pattern correlated strongly with intra-cerebellar functional connectivity. Of these genes, 90 were also differentially expressed in the cerebral cortex and linked the cortico-cerebellar cognitive-limbic networks. To further discover the biological functions of these genes, we performed a virtual gene knock-out by observing the change in the coupling between gene co-expression and functional connectivity and divided the genes into two subsets, i.e., a positive gene contribution indicator (GCI+) and a negative gene set (GCI-). GCI+ is mainly involved in cerebellar neurodevelopment, while GCI- is related to neurotransmission and is significantly enriched in various neurological and neuropsychiatric disorders that are closely linked the cerebellar functional abnormalities. Collectively, our results provide new insight into the genetic substrates behind the functional organization of the human cerebellum with relevance to the possible mechanism of cerebellar contributions to related neurological and psychiatric disorders.