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Cotton <i>Verticillium</i> wilt, caused by the notorious fungal phytopathogen <i>Verticillium dahliae</i> (<i>V.</i> <i>dahliae</i>), is a destructive soil-borne vascular disease and severely decreases cotton yield and quality worldwide. Transcriptional and post-transcriptional regulation of genes responsive to <i>V.</i> <i>dahliae</i> are crucial for <i>V.</i> <i>dahliae</i> tolerance in plants. However, the specific microRNAs (miRNAs) and the miRNA/target gene crosstalk involved in cotton resistance to <i>Verticillium</i> wilt remain largely limited. To investigate the roles of regulatory RNAs under <i>V.</i> <i>dahliae</i> induction in upland cotton, mRNA and small RNA libraries were constructed from mocked and infected roots of two upland cotton cultivars with the <i>V.</i> <i>dahliae</i>-sensitive cultivar Jimian 11 (J11) and the <i>V.</i> <i>dahliae</i>-tolerant cultivar Zhongzhimian 2 (Z2). A comparative transcriptome analysis revealed 8330 transcripts were differentially expressed under <i>V.</i> <i>dahliae</i> stress and associated with several specific biological processes. Moreover, small RNA sequencing identified a total of 383 miRNAs, including 330 unique conserved miRNAs and 53 novel miRNAs. Analysis of the regulatory network involved in the response to <i>V.</i> <i>dahliae</i> stress revealed 31 differentially expressed miRNA–mRNA pairs, and the up-regulation of GhmiR395 and down-regulation of GhmiR165 were possibly involved in the response to <i>V. dahliae</i> by regulating sulfur assimilation through the GhmiR395-<i>APS1/3</i> module and the establishment of the vascular pattern and secondary cell wall formation through GhmiR165-<i>REV</i> module, respectively. The integrative analysis of mRNA and miRNA expression profiles from upland cotton lays the foundation for further investigation of regulatory mechanisms of resistance to <i>Verticillium</i> wilt in cotton and other crops.