The major component of complex genomes is repetitive elements, which remain recalcitrant to characterization. Using maize as a model system, we analyzed whole genome shotgun (WGS) sequences for the two maize inbred lines B73 and Mo17 using k-mer analysis to quantify the differences between the two genomes. Significant differences were identified in highly repetitive sequences, including centromere repeats, 45S ribosomal DNA (rDNA), knob, and telomere repeats. Previously unknown genotype specific 45S rDNA sequences were discovered. The B73-specific 45S rDNA is not only located on the nucleolus organizer region (NOR) on chromosome 6 but also dispersed on all the chromosomes in B73, indicating the relatively recent spread of 45S rDNA from the NOR. The B73 and Mo17 polymorphic k-mers were used to examine allele-specific expression of 45S rDNA. Although Mo17 contains higher copy number than B73, equivalent levels of overall 45S rDNA expression indicates that dosage compensation operates for the 45S rDNA in the hybrids. Using WGS sequences of B73xMo17 double haploids (DHs), genomic locations showing differential repetitive contents were genetically mapped. Analysis of WGS sequences of HapMap2 lines, including maize wild progenitor teosintes, landraces, and improved lines, decreases and increases in abundance of additional sets of k-mers associated with centromere repeats, 45S rDNA, knob, and retrotransposon sequences were found between teosinte and maize lines, revealing global evolutionary trends of genomic repeats during maize domestication and improvement.