9DNA methylation is an important chromatin modification that can stably alter gene expression in 10 cells and maintain genome integrity in plants and vertebrates. The function of DNA methylation 11 outside of these well-studied systems, however, is unclear. Insects, in particular, represent an 12 understudied group. Variation in the level of DNA methylation and gains and losses in the 13 maintenance methyltransferase, DNMT1, across the insect tree of life suggests that there is much we 14don't understand about DMNT1 function and evolution. One constant across the studies examining 15 patterns of Dnmt1 expression in insects is that expression is consistently high in reproductive tissues 16 compared to somatic tissue. The explanation for this has been that DNMT1 is required in tissues that 17have high levels of cell division. Our previous study found that downregulation of Dnmt1 expression 18 in the milkweed bug Oncopeltus fasciatus results in the expected reduction of DNA methylation, no 19global changes in gene expression reflecting changes in DNA methylation, and the loss of the ability 20 to produce viable oocytes. Here, we show that females treated with ds-Dnmt1 RNA during larval 21 development have a more extreme phenotype; they lack oocytes entirely but develop a normal 22 somatic ovary. Our results indicate a specific role for DNMT1 in the formation of gametes and are 23 consistent with data from other systems, including Tribolium castaneum, a species does not have 24 DNA methylation. We propose that DNMT1 has multiple functional roles in addition to methylating 25 DNA, which explains its complex patterns of evolution, and suggests that previous inferences of 26 causation from associations are premature. 27