How do growth hormones interact to specify female-germline cell types in flowering plants and control production of the first female-germline cell? Here, we find that gibberellin (GA) biosynthesis and signaling are restricted in ovule primordia, with overexpression of receptors and biosynthetic enzymes resulting in multiple and enlarged megaspore mother cells (MMCs) in Arabidopsis. GA signaling machinery interacts with and promotes the degradation of cytokinin (CK) type-B Arabidopsis response regulators (ARR1/10/12), which also directly interact with DELLA proteins. CK biosynthesis and signaling components are expressed in both MMCs and sporophytic cells, with signaling negatively controlled by GA in ovule primordia, and perturbations leading to the induction of multiple, enlarged MMC-like cells. The vacuolar sorting protein SHRUBBY (SHBY) interacts with GA and CK signaling components to block GA-induced degradation. CK signaling restricts multiple sub-epidermal cells in distal ovule primordia from acquiring MMC identity. By balancing degradation activity, GA and CK signaling antagonistically control female-germline cell specification.