Arbuscular mycorrhizal (AM) symbiosis is known to stimulate plant drought tolerance. However, the mechanisms underlying the synergistic responses of the symbiotic partners to drought stress are largely unknown. A split-root experiment was designed to investigate the molecular interactions between a host plant and an AM fungus (AMF) under drought stress. In the two-compartment cultivation system, an entire or only a half root system of a maize plant was inoculated with an AMF, Rhizophagus intraradices, in the presence of localized or systemic drought treatment. Plant physiological parameters including growth, water status, and phosphorus concentration, and the expression of drought tolerance-related genes in both roots and R. intraradices were recorded. Although mycorrhizal inoculation in either one or both compartments systemically decreased abscisic acid (ABA) content in the whole root system subjected to systemic or local drought stress, we observed local and/or systemic AM effects on root physiological traits and the expression of functional genes in both roots and R. intraradices. Interestingly, the simultaneous increase in the expression of plant genes encoding D-myo-inositol-3-phosphate synthase (IPS) and 14-3-3-like protein GF14 (14-3GF), which were responsible for ABA signal transduction, was found to be involved in the activation of 14-3-3 protein and aquaporins (GintAQPF1 and GintAQPF2) in R. intraradices. These findings suggest that coexpression of IPS and 14-3GF is responsible for the crosstalk between maize and R. intraradices under drought stress, and potentially induces the synergistic actions of the symbiotic partners in enhancing plant drought tolerance.