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Abstract Transposable elements (TEs), despite generally being considered deleterious, represent a substantial portion of most eukaryotic genomes. Specific genomic regions, such as telomeres and pericentromeres, are often densely populated with TEs. In these regions, which tend to be gene-poor, reduced recombination shelters the genome from the deleterious effects of TEs. Here, we describe unusually large and continuous pericentromeric transposable element-rich regions in all chromosomes of the genome assembly of Pegoscapus hoffmeyeri sp. A (511.79 Mbp), a Neotropical fig wasp that is the obligate pollinator of Ficus obtusifolia. The identified pericentromeric transposable element-rich regions span nearly half (46%) of the genome, and harbor over 40% of all annotated genes, including 30% of conserved Benchmarking Universal Single-Copy Orthologs genes. We present evidence that low recombination in these transposable element-rich regions generates strong bimodal molecular evolution patterns genome-wide. Patterns of nucleotide diversity and protein-coding gene evolution in transposable element-rich regions are consistent with a reduced efficiency of selection and suggestive of strong Hill–Robertson effects. A significant reduction in third codon position GC content (GC3) in transposable element-rich regions emerged as the most distinctive gene feature differentiating genes in transposable element-rich regions from those in the rest of the genome, a pattern that likely results from the absence of GC-biased gene conversion. This remarkable bimodal compartmental genome organization in the genome of P. hoffmeyeri provides a unique example of how genome organization with compartmental transposable element distribution can lead to context-dependent gene evolution shaped by common evolutionary forces.