Progesterone receptor (PGR) is a hormone-responsive transcription factor with important roles in regulating transcription in the female reproductive tract. In the ovary, PGR is critical for ovulation and female fertility. The underlying molecular mechanism of PGR ovulatory action is of particular interest for the development of safer non-hormonal female contraceptives. We showed that PGR possesses unique cistromic and transcriptomic properties in different female reproductive tissues; particularly in ovarian granulosa cells, PGR transcriptional regulatory action does not rely on the canonical pathway that involves binding at DNA sequences with the PGR response element (PRE) motif. To further elucidate the molecular mechanism behind ovarian PGR action, we generated and integrated ATAC-seq, ChIP-seq and RNA-seq data from mouse granulosa cells in response to in vivo ovulatory hormone stimulation and in the absence of PGR through a PGR knockout mouse model. ATAC-seq of granulosa cells with or without ovulatory stimulation confirms that chromatin sites bearing the PRE motif are indeed significantly less accessible post-stimulation; instead, PGR ovarian action is mainly driven by interaction with specific transcription factor partners, including RUNX1, at non-canonical chromatin sites. RUNX1 ChIP-seq analysis shows that PGR and RUNX1 cistromes overwhelmingly overlap at transcriptionally active promoters. PGR and RUNX1 also co-interact with distal ovarian enhancers that are associated with ovulatory genes. Another transcriptional regulatory mechanism of PGR involves PGR directly promoting the accessibility of target promoters and enhancers through interaction with the canonical PRE motif, shown through ATAC-seq and RNA-seq in PGR wildtype vs knockout mice. Overall, we show that by employing two distinct mechanisms – direct interaction with RUNX1 at non-canonical regulatory elements, and chromatin remodeling at canonical PGR binding sites – PGR regulates a specific suite of chromatin targets that is critical for the ovulatory transcriptional network.