The transcription factor FOXL2 is required in ovarian somatic cells for female fertility. Differential timing of Foxl2 deletion, in embryonic versus adult mouse ovary, leads to distinctive outcomes suggesting different roles across development. Here, we comprehensively investigated FOXL2’s role through a multi-omics approach including chromatin proteomics, transcriptomics, ATAC-Seq and ChIP-Seq. We characterised gene expression dynamics and chromatin accessibility changes, coupled with genome-wide identification of FOXL2 targets and on-chromatin interacting partners in somatic cells across ovarian development. We found that FOXL2 regulates more targets postnatally, through interaction with factors regulating primordial follicle formation and steroidogenesis. One of these interactors was USP7, which plays a role in chromatin remodelling through its histone deubiquitination activity, which can affect gene transcription activation and silencing. We found that USP7 is necessary for the differentiation and proliferation of the somatic cell lineages of the ovary. Deletion of USP7 results in impairment of somatic cell differentiation, germ cell nest breakdown and ovarian development, leading to sterility. Our datasets constitute a comprehensive resource for exploration of the molecular mechanisms of ovarian development and causes of female infertility.