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<i>Verticillium</i> wilt, primarily induced by the soil-borne fungus <i>Verticillium dahliae</i>, is a serious threat to cotton fiber production. There are a large number of <i>really interesting new gene</i> (RING) domain-containing E3 ubiquitin ligases in Arabidopsis, of which three (At2g39720 (AtRHC2A), At3g46620 (AtRDUF1), and At5g59550 (AtRDUF2)) have a domain of unknown function (DUF) 1117 domain in their C-terminal regions. This study aimed to detect and characterize the RDUF members in cotton, to gain an insight into their roles in cotton’s adaptation to environmental stressors. In this study, a total of 6, 7, 14, and 14 <i>RDUF</i> (<i>RING-DUF1117</i>) genes were detected in <i>Gossypium arboretum</i>, <i>G. raimondii</i>, <i>G. hirsutum</i>, and <i>G. barbadense</i>, respectively. These <i>RDUF</i> genes were classified into three groups. The genes in each group were highly conserved based on gene structure and domain analysis. Gene duplication analysis revealed that segmental duplication occurred during cotton evolution. Expression analysis revealed that the <i>GhRDUF</i> genes were widely expressed during cotton growth and under abiotic stresses. Many <i>cis</i>-elements related to hormone response and environment stressors were identified in GhRDUF promoters. The predicted target miRNAs and transcription factors implied that <i>GhRDUF</i><i>s</i> might be regulated by gra-miR482c, as well as by transcription factors, including MYB, C2H2, and Dof. The <i>GhRDUF</i> genes responded to cold, drought, and salt stress and were sensitive to jasmonic acid, salicylic acid, and ethylene signals. Meanwhile, <i>GhRDUF4D</i> expression levels were enhanced after <i>V. dahliae</i> infection. Subsequently, <i>GhRDUF4D</i> was verified by overexpression in <i>Arabidopsis</i> and virus-induced gene silencing treatment in upland cotton. We observed that <i>V</i>. <i>dahliae</i> resistance was significantly enhanced in transgenic <i>Arabidopsis</i>, and weakened in <i>GhRDUF4D</i> silenced plants. This study conducted a comprehensive analysis of the <i>RDUF</i> genes in <i>Gossypium</i>, hereby providing basic information for further functional studies.