Context.— Tumors harboring CIC-NUTM1 fusion are a newly recognized rare sarcoma, but the documented cases are still limited. It is unclear whether it is the same as classic CIC-DUX4 sarcoma in terms of its clinical, pathologic, and behavioral aspects. Objective.— To further explore the clinicopathologic characteristics of CIC-NUTM1 sarcoma. Design.— The cases were diagnosed based on immunophenotype, next-generation sequencing, and fluorescence in situ hybridization tests and compared with the reported CIC-NUTM1 sarcomas in the literature. Results.— Three cases of CIC-NUTM1 sarcomas involving the spine in adults were described. They were 2 men and 1 woman, aged 38 to 61 years. Two tumors were located in thoracic vertebrae and 1 in a cervical vertebra. All were locally advanced lesions destroying the bone and soft tissues without spinal cord involvement or metastasis. The tumors were composed of monomorphic small to medium-sized cells with round to epithelioid appearance. The architecture was lobulated and solid with diffuse or multifocal myxoid stroma. Next-generation sequencing revealed an in-frame fusion between CIC (exon 16 or 17) and NUTM1 (exon 5 or 6) in 3 cases. Fluorescence in situ hybridization confirmed CIC and NUTM1 breaks, and immunohistochemistry showed NUT staining in the nucleus. The patients died of disease 8 to 15 months (mean, 10.7 months) after presentation. Of the CIC-NUTM1 sarcomas reported in the literature along with our cases (n = 11), 8 cases developed in axial bone (5 spine, 3 skull base). Conclusions.— CIC-NUTM1 sarcomas showed distinct anatomic tropism for the axial skeleton and unfavorable behavior compared with classic CIC sarcoma.