Ribosomal RNA genes (rRNAs) are encoded in the genome in hundreds of copies (rDNA) to satisfy the high demand for ribosomes in a cell. However, due to its repetitive nature, the rDNA remains the most recalcitrant region to genome assembly, and it is generally assumed that all repeat copies are identical to each other. Moreover, most studies have been based on short-read sequencing using a consensus sequence for a single repeat unit. Consequently, little is known about the variation of the rDNA and its consequences for ribosome activity. We have devised an innovative approach that leverages Nanopore long reads to investigate the properties of the rDNA repeat arrays. Using sequencing data from the lymphoblastoid cell line (LCL) GM24385 we identified 918 reads of length >100kb containing a total of 3300 candidate rDNA repeat units (average 3-4 units per read). The rDNA units had highly conserved sizes, suggesting that most rDNA units have full coding potential. We performed direct RNA sequencing of rRNAs from the cytosolic fraction of the same cell line (LCL) and found that 99 of the rDNA variants were expressed in rRNAs. We further found two starkly contrasting methylation patterns of CpG methylation on the rDNA repeats occurring in similar proportions (~50% each). One with the rRNA genes and promoter unmethylated and the IGS highly methylated and the other with the rRNA genes, the promoter, and the IGS highly methylated. Strikingly, most (~90%) of the 918 reads analyzed had the same methylation pattern in all units, rather than alternating between methylated and unmethylated. Moreover, we found reads with inversions resulting in units with diverging and converging transcriptional orientations. The variation in sequence, structure, and methylation we have uncovered represent previously unrecognized ways through which the rDNA may influence ribosome rRNA composition and cell function.