Recently, a renewed interest in cytokinins (CKs) has allowed the characterization of these phytohormones as key regulatory molecules in plant biotic interactions. They have been proved to be instrumental in microbe- and insect-mediated plant phenotypes that can be either beneficial or detrimental for the host-plant. In parallel, insect endosymbiotic bacteria have emerged as key players in plant-insect interactions mediating directly or indirectly fundamental aspects of insect nutrition, such as insect feeding efficiency or the ability to manipulate plant physiology to overcome food nutritional imbalances. However, mechanisms that regulate CK production and the role played by insects and their endosymbionts remain largely unknown. Against this backdrop, studies on plant-associated bacteria have revealed fascinating and complex molecular mechanisms that lead to the production of bacterial CKs and the modulation of plant-borne CKs which ultimately result in profound metabolic and morphological plant modifications. This review highlights major strategies used by plant-associated bacteria that impact the CK homeostasis of their host-plant, to raise parallels with strategies used by phytophagous insects and to discuss the possible role played by endosymbiotic bacteria in these CK-mediated plant phenotypes. We hypothesize that insects employ a CK-mix production strategy that manipulates the phytohormonal balance of their host-plant and overtakes plant gene expression causing a metabolic and morphological habitat modification. In addition, insect endosymbiotic bacteria may prove to be instrumental in these manipulations through the production of bacterial CKs, including specific forms that challenge the CK-degrading capacity of the plant (thus ensuring persistent effects) and the CK-mediated plant defenses.