Meiotic drivers are selfish genes that bias their transmission into gametes, defying Mendelian inheritance. Despite the significant impact of these genomic parasites on evolution and infertility, few meiotic drive loci have been identified or mechanistically characterized. Here, we demonstrate a complex landscape of meiotic drive genes on chromosome 3 of the fission yeasts  Schizosaccharomyces kambucha  and  S. pombe . We identify  S. kambucha wtf4  as one of these genes that acts to kill gametes (known as spores in yeast) that do not inherit the gene from heterozygotes.  wtf4  utilizes dual, overlapping transcripts to encode both a gamete-killing poison and an antidote to the poison. To enact drive, all gametes are poisoned, whereas only those that inherit  wtf4  are rescued by the antidote. Our work suggests that the  wtf  multigene family proliferated due to meiotic drive and highlights the power of selfish genes to shape genomes, even while imposing tremendous costs to fertility.