Progesterone is critical for many aspects of female reproduction such as ovulation, oviductal transport, implantation, and maintenance of pregnancy. Its effects are mediated by the progesterone receptor (PGR), which occurs in both PGR-A and PGR-B isoforms, acting as nuclear hormone transcription factors. In the ovary, PGR is transiently expressed, specifically in granulosa cells of preovulatory follicles in response to the luteinizing hormone (LH) surge that triggers ovulation. To identify PGR regulated genes that are responsible for these key reproductive events we conducted microarray analyses of mRNA from granulosa cells and oviducts comparing progesterone receptor null mice (PRKOs) and heterozygous littermates. Microarray results confirmed that proteases Adamts1 and Cathepsin L are expressed at greatly reduced levels in PRKO granulosa cells, and identified novel gene products involved in cellular migration and invasion processes that are likely to mediate the dynamic tissue remodeling that facilitates ovulation. In the oviduct, PGR is expressed predominantly in luminal epithelial cells but also muscle cells. A large number of oviductal genes were also dysregulated in PRKO mouse oviducts during the peri-ovulatory period and we identified and subsequently validated several that have potential roles in cumulus-oocyte capture and transport following ovulation. The majority were genes associated with adhesion and muscular contractility including integrin α 8, endothelin 3, myocardin and angiotensin II receptor. Thus, the actions of PGR play key roles in coordinating the functions of multiple tissues, including the important peri-ovulatory events of oocyte release and acquisition of oocyte developmental competence, as well as subsequent oviductal transport of the newly formed embryo and immunological events at implantation.