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Abscisic acid (ABA) plays an important role in the regulation of plant adaptation, seed germination, and root development in plants. However, the mechanism of ABA regulation of root development is still poorly understood, especially through the miRNA-mediated pathway. Here, small RNA (sRNA)-seq and degradome-seq were used to analyze the miRNAs’ responsive to ABA in the stems and roots of P. euphratica, a model tree species for abiotic stress-resistance research. In total, 255 unique mature sequences, containing 154 known miRNAs and 101 novel miRNAs were identified, among which 33 miRNAs and 54 miRNAs were responsive to ABA in the roots and stems, respectively. Furthermore, the analysis of these miRNAs and their targets revealed a new hormone signaling crosstalk model of ABA regulation of root growth through miRNA-mediated pathways, such as peu-miR-n68 mediation of the crosstalk between ABA and the brassinosteroid (BR) signaling pathway and peu-miR477b mediation of the crosstalk between ABA and Gibberellic acid (GA) signaling. Taken together, our genome-wide analysis of the miRNAs provides a new insight into the mechanism of ABA regulation of root growth in Populus.