Selfish genetic elements use a myriad of mechanisms to drive their inheritance and ensure their survival into the next generation, often at a fitness cost to its host.1,2 Although the catalog of selfish genetic elements is rapidly growing, our understanding of host drive suppression systems that counteract self-seeking behavior is lacking. Here, we demonstrate that the biased transmission of the non-essential, non-driving B chromosomes in Drosophila melanogaster can be achieved in a specific genetic background. Combining a null mutant of matrimony, a gene that encodes a female-specific meiotic regulator of Polo kinase,3,4 with the TM3 balancer chromosome creates a driving genotype that is permissive for the biased transmission of the B chromosomes. This drive is female-specific, and both genetic components are necessary, but not individually sufficient, for permitting a strong drive of the B chromosomes. Examination of metaphase I oocytes reveals that B chromosome localization within the DNA mass is mostly abnormal when drive is the strongest, indicating a failure of the mechanism(s) responsible for the proper distribution of B chromosomes. We propose that some proteins important for proper chromosome segregation during meiosis, like Matrimony, may have an essential role as part of a meiotic drive suppression system that modulates chromosome segregation to prevent genetic elements from exploiting the inherent asymmetry of female meiosis. Display omitted •Female meiotic drive promotes biased B chromosome inheritance in D. melanogaster•A genetic reduction of Mtrm and the TM3 balancer chromosome are necessary for drive•Strong drive correlates with aberrant B chromosome arrangements during metaphase I•The distributive segregation system may act to suppress drive during female meiosis B chromosomes are genetic renegades that can rapidly spread through a population when left unchecked. Hanlon and Hawley show that the B chromosomes in D. melanogaster are subject to female meiotic drive in a specific mutant, leading to the identification of a drive suppression system that may protect against invasion by selfish genetic elements.