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Cyclic nucleotide-gated channels (CNGCs) constitute a family of non-selective cation channels that are primarily permeable to Ca²⁺ and activated by the direct binding of cyclic nucleotides (i.e., cAMP and cGMP) to mediate cellular signaling, both in animals and plants. Until now, our understanding of CNGCs in cotton (<i>Gossypium</i> spp.) remains poorly addressed. In the present study, we have identified 40, 41, 20, 20, and 20 CNGC genes in <i>G. hirsutum</i>, <i>G. barbadense</i>, <i>G. herbaceum</i>, <i>G. arboreum</i>, and <i>G. raimondii</i>, respectively, and demonstrated characteristics of the phylogenetic relationships, gene structures, chromosomal localization, gene duplication, and synteny. Further investigation of CNGC genes in <i>G. hirsutum</i>, named <i>GhCNGC1-40</i>, indicated that they are not only extensively expressed in various tissues and at different developmental stages, but also display diverse expression patterns in response to hormones (abscisic acid, salicylic acid, methyl jasmonate, ethylene), abiotic (salt stress) and biotic (<i>Verticillium dahlia</i> infection) stimuli, which conform with a variety of <i>cis</i>-acting regulatory elements residing in the promoter regions; moreover, a set of <i>GhCNGCs</i> are responsive to cAMP signaling during cotton fiber development. Protein–protein interactions supported the functional aspects of <i>GhCNGCs</i> in plant growth, development, and stress responses. Accordingly, the silencing of the homoeologous gene pair <i>GhCNGC1</i>&<i>18</i> and <i>GhCNGC12</i>&<i>31</i> impaired plant growth and development; however, <i>GhCNGC1</i>&<i>18</i>-silenced plants enhanced <i>Verticillium</i> wilt resistance and salt tolerance, whereas <i>GhCNGC12</i>&<i>31</i>-silenced plants had opposite effects. Together, these results unveiled the dynamic expression, differential regulation, and functional diversity of the CNGC family genes in cotton. The present work has laid the foundation for further studies and the utilization of <i>CNGCs</i> in cotton genetic improvement.