Irx3 and Irx5 are critical transcription factors necessary for ovarian follicle development in the mouse. The knockout of Irx3 and Irx5 results in marked oocyte death, which is a feature common to Wnt/-catenin knockout ovaries. Canonical Wnt/-catenin are crucial factors involved in ovarian development and this similar phenotype suggests a link between Irx3 and Irx5 and this pathway. Irx3 has been used as a marker for canonical Wnt signaling in several tissues, including the developing ovary; however, the mechanism by which regulation occurs is unclear. I hypothesized that -catenin binds Wnt-responsive enhancer elements via TCF/LEF family members to stimulate Irx3 and Irx5 in the developing ovary. DNaseI-seq and ATAC-seq data helped identify potential regulatory elements in the somatic cell population of developing gonads, and I discovered two regions within the IrxB locus that may function as -catenin responsive enhancers that stimulate Irx3 and Irx5 in ovarian development. Repressive histone marker H3K27me3 may also play a role in the repression of these enhancers in the testis, suggesting that histone modifications and -catenin/TCF/LEF are regulating Irx3 and Irx5 expression in developing gonads at both the epigenetic and transcriptional levels. We also have evidence to support that Irx3 plays a critical role in the germ cell of the ovary. While I showed Irx3 and Irx5 are regulated by canonical Wnt/-catenin signaling in the somatic cells, I hypothesized whether their regulatory mechanism is consistent in the oocyte. With the use of a newly developed germ-cell specific cre FiglaCre-EGFP, I was able to eliminate -catenin in the oocyte of the ovary at an early postnatal stage. IRX3 expression in the oocyte is not affected by the loss of -catenin, indicating the regulation of Irx3 in the oocyte differs from that in the somatic cells. Loss of -catenin in the oocyte, additionally, does not affect ovarian development or follicle maturation, suggesting loss of -catenin is not critical for ovarian health. Irx3 has a dynamic expression profile in the ovary, where it is expressed in both somatic and germ cells at different points during development. Prior to primordial follicle formation, Irx3 is confined to the somatic (pre-granulosa) cells of germline nests. After germline nest breakdown and primordial follicle formation, however, Irx3 is expressed in the oocyte and remains in the oocyte into adulthood. My goal was to stabilize Irx3 in the somatic cells in the ovary after expression would normally migrate to the germ cell, or to overexpress Irx3 in the oocyte to explore if Irx3 overexpression would affect ovarian health or female fertility. I can conclude that overexpression of Irx3 in either the somatic or germ cells of the ovary does not affect ovarian morphology during development and adulthood and that these females are viable and fertile. In addition, I also introduced Irx3 in the testis in both somatic and germ cells where it is normally absent at all stages of development. While somatic cell Irx3 overexpression did not affect testis histology or male fertility, germ cell Irx3 overexpression revealed these males were sub-fertile and displayed a sperm agglutination phenotype. Irx3 overexpression has yet to be connected to male infertility and warrants further investigation into the pathogenesis of this phenotype. Altogether, I was able to elucidate the regulatory mechanism for Irx3 and Irx5 in the somatic cells of the ovary while I also discovered that this mechanism does not translate to the neighboring oocyte. Next, I showed that Irx3 overexpression in the ovary does not affect ovarian function, while germ cell overexpression of Irx3 produces as unique phenotype in male mice. This work expands our understanding and opens new avenues of research for the study of Irx3 and Irx5 in gonad development and how the regulation of these factors may contribute to fertility defects in humans.