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Meiosis is generally a fair process: each chromosome has a 50% chance of being included into each gamete. However, meiosis can become aberrant with some chromosomes having a higher chance of making it into gametes than others. Yet, why and how such systems evolve remains unclear. Here, we study the unusual reproductive genetics of mealybugs, where only maternal-origin chromosomes are included in gametes during male meiosis, while paternal chromosomes are eliminated. One species-Pseudococcus viburni-has a segregating B chromosome that drives by escaping paternal genome elimination. We present whole genome and gene expression data from lines with and without B chromosomes. We identify B-linked sequences including 204 protein-coding genes and a satellite repeat that makes up a significant proportion of the chromosome. The few paralogs between the B and the core genome are distributed throughout the genome, arguing against a simple, or at least recent, chromosomal duplication of one of the autosomes to create the B. We do, however, find one 373 kb region containing 146 genes that appears to be a recent translocation. Finally, we show that while many B-linked genes are expressed during meiosis, most of these are encoded on the recently translocated region. Only a small number of B-exclusive genes are expressed during meiosis. Of these, only one was overexpressed during male meiosis, which is when the drive occurs: an acetyltransferase involved in H3K56Ac, which has a putative role in meiosis and is, therefore, a promising candidate for further studies., (© The Author(s) 2025. Published by Oxford University Press on behalf of Society for Molecular Biology and Evolution.)