Carotenoids are a large class of isoprenoid compounds which are biosynthesized by plants, algae, along with certain fungi, bacteria and insects. In plants, carotenoids provide crucial functions in photosynthesis and photoprotection. Furthermore, carotenoids also serve as precursors to apocarotenoids, which are derived through enzymatic and non-enzymatic cleavage reactions. Apocarotenoids encompass a diverse set of compounds, including hormones, growth regulators, and signaling molecules which play vital roles in pathways associated with plant development, stress responses, and plant-organismic interactions. Regulation of carotenoid biosynthesis indirectly influences the formation of apocarotenoids and bioactive effects on target pathways. Recent discovery of a plethora of new bioactive apocarotenoids across kingdoms has increased interest in expanding knowledge of the breadth of apocarotenoid function and regulation. In this review, we provide insights into the regulation of carotenogenesis, specifically linked to the biosynthesis of apocarotenoid precursors. We highlight plant studies, including useful heterologous platforms and synthetic biology tools, which hold great value in expanding discoveries, knowledge and application of bioactive apocarotenoids for crop improvement and human health. Moreover, we discuss how this field has recently flourished with the discovery of diverse functions of apocarotenoids, thereby prompting us to propose new directions for future research.