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 TE-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 TE-rich regions span nearly half (46%) of the genome, and harbor over 40% of all annotated genes, including 30% of conserved BUSCO genes. We present evidence that low recombination in these TE-rich regions generates strong bimodal molecular evolution patterns genome wide. Patterns of nucleotide diversity and protein-coding gene evolution in TE-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 TE-rich regions emerged as the most distinctive gene feature differentiating genes in TE-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 TE distribution can lead to context-dependent gene evolution shaped by common evolutionary forces.