Of the array of spontaneous mutations that can occur, changes to chromosome number may have the greatest impact on the evolutionary potential of populations and the condition of affected individuals. Chromosomal nondisjunction resulting in aneuploidy is found across eukaryotes, but the consequences of such karyotypic variation have not been widely explored. In the fruit fly Drosophila melanogaster, aneuploid females with an XXY karyotype can arise through nondisjunction, inheriting a Y chromosome from their male parent. While the Y chromosome contains few genes, the large amount of heterochromatic DNA it contains can substantially alter genome-wide gene expression in females. We conducted a series of experiments to understand how sex chromosome aneuploidy alters key traits in affected females and their progeny. In the same genetic background, we also determined the rate at which this karyotype appears spontaneously and its standing frequency. We found that XXY females largely resembled XX females, but experienced size and fecundity benefits when receiving a male-transmitted Y chromosome. However, XYY males produced by aneuploid females experienced reduced viability, limiting the standing frequency of aneuploidy at mutation-selection equilibrium. Our findings demonstrate that aneuploid flies are not too rare in laboratory populations, but that the effects of this karyotypic diversity depend on sex and parent of origin.