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Calcineurin B-like protein-interacting protein kinases (<i>CIPKs</i>), as key regulators, play an important role in plant growth and development and the response to various stresses. In the present study, we identified 80 and 78 <i>CIPK</i> genes in the <i>Gossypium hirsutum</i> and <i>G. barbadense</i>, respectively. The phylogenetic and gene structure analysis divided the cotton <i>CIPK</i> genes into five groups which were classified into an exon-rich clade and an exon-poor clade. A synteny analysis showed that segmental duplication contributed to the expansion of <i>Gossypium CIPK</i> gene family, and purifying selection played a major role in the evolution of the gene family in cotton. Analyses of expression profiles showed that <i>GhCIPK</i> genes had temporal and spatial specificity and could be induced by various abiotic stresses. Fourteen <i>GhCIPK</i> genes were found to contain 17 non-synonymous single nucleotide polymorphisms (SNPs) and co-localized with oil or protein content quantitative trait loci (QTLs). Additionally, five SNPs from four <i>GhCIPKs</i> were found to be significantly associated with oil content in one of the three field tests. Although most <i>GhCIPK</i> genes were not associated with natural variations in cotton oil content, the overexpression of the <i>GhCIPK6</i> gene reduced the oil content and increased C18:1 and C18:1+C18:1d6 in transgenic cotton as compared to wild-type plants. In addition, we predicted the potential molecular regulatory mechanisms of the <i>GhCIPK</i> genes. In brief, these results enhance our understanding of the roles of <i>CIPK</i> genes in oil synthesis and stress responses.