Cytokinins have many essential roles in embryonic and post-embryonic growth and development, but their role in fruit morphogenesis is currently not really known. Moreover, information about the spatio-temporal localization pattern of cytokinin signaling in gynoecia and fruits is lacking. Therefore, the synthetic reporter line TCS::GFP was used to visualize cytokinin signaling during gynoecium and fruit development. Fluorescence was detected at medial regions of developing gynoecia, and, unexpectedly, at the valve margin in developing fruits, and was severely altered in mutants that lack or ectopically acquire valve margin identity. Comparison to developing gynoecia and fruits in a DR5rev::GFP line showed that the transcriptional responses to cytokinin and auxin are frequently present in complementary patterns. Moreover, cytokinin treatments in early gynoecia produced conspicuous changes, and treatment of valve margin mutant fruits restored this tissue. The results suggest that the phytohormone cytokinin is important in gynoecium and fruit patterning and morphogenesis, playing at least two roles: an early proliferation-inducing role at the medial tissues of the developing gynoecia, and a late role in fruit patterning and morphogenesis at the valve margin of developing fruits.