The B-chromosome of maize contains an A-chromosome centromere-specific satellite CentC repeat in its centromere region (CENB) and at multiple locations in its distal heterochromatic regions (BDHs). Because CentC is highly repetitive, it is a challenge to study CentC sequences within individual centromeres or chromosome regions. The combined structure of CentC and a BDH-specific CL-repeat has allowed us to isolate CentC sequences from BDHs. In the study described herein, we have used a PCR method to amplify 13 CL-CentC variant products that were specifically mapped to A-centromeres (CENAs), the CENB, and BDHs via the tertiary trisomes and hypoploids of five B-10L translocations. Cloning and sequence analyses of these CL-CentC products have revealed a local CentC homogenization within the three CentC-containing regions. Phylogenetic analysis has indicated that the CentC sequences of BDHs are more closely related to those of CENAs in comparison to that of the CENB. Furthermore, the CentC monomers that are within the CENB are more diverse than those within BDHs and CENAs. These results shed light on the evolution of CentC repeats on the B-chromosome and provide a better understanding of B-chromosome evolution.