Multicellular organisms, such as plants, fungi, and animals, develop organs with specialized functions. Major challenges in developing such structures include establishment of polarity along three axes (apical-basal, medio-lateral, and dorso-ventral/abaxial-adaxial), specification of tissue types and their coordinated growth, and maintenance of communication between the organ and the entire organism. The gynoecium of the model plant Arabidopsis thaliana embodies the female reproductive organ and has proven an excellent model system for studying organ establishment and development, given its division into different regions with distinct symmetries and highly diverse tissue types. Upon pollination, the gynoecium undergoes dramatic changes in morphology and developmental programming to form the seed-containing fruit. In this review, we wish to provide a detailed overview of the molecular and genetic mechanisms that are known to guide gynoecium and fruit development in A. thaliana. We describe networks of key genetic regulators and their interactions with hormonal dynamics in driving these developmental processes. The discoveries made to date clearly demonstrate that conclusions drawn from studying gynoecium and fruit development in flowering plants can be used to further our general understanding of organ formation across the plant kingdom. Importantly, this acquired knowledge is increasingly being used to improve fruit and seed crops, facilitated by the recent profound advances in genomics, cloning, and gene-editing technologies.