Studies in laboratory models and postmortem human brain tissue from patients with Alzheimer's disease have revealed disruption of basic cellular processes such as DNA repair and epigenetic control as drivers of neurodegeneration. While genomic alterations in regions of the genome that are rich in repetitive sequences, often termed "dark regions," are difficult to resolve using traditional sequencing approaches, long-read technologies offer promising new avenues to explore previously inaccessible regions of the genome. In the current study, we leverage nanopore-based long-read whole-genome sequencing of DNA extracted from postmortem human frontal cortex at early and late stages of Alzheimer's disease, as well as age-matched controls, to analyze retrotransposon insertion events, non-allelic homologous recombination (NAHR), structural variants and DNA methylation within retrotransposon loci and other repetitive/dark regions of the human genome. Interestingly, we find that retrotransposon insertion events and repetitive element-associated NAHR are particularly enriched within centromeric and pericentromeric regions of DNA in the aged human brain, and that ribosomal DNA (rDNA) is subject to a high degree of NAHR compared to other regions of the genome. We detect a trending increase in potential somatic retrotransposition events of the small interfering nuclear element (SINE) AluY in late-stage Alzheimer's disease, and differential changes in methylation within repetitive elements and retrotransposons according to disease stage. Taken together, our analysis provides the first long-read DNA sequencing-based analysis of retrotransposon sequences, NAHR, structural variants, and DNA methylation in the aged brain, and points toward transposable elements, centromeric/pericentromeric regions and rDNA as hotspots for genomic variation.