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<i>WUSCHEL</i>-related homeobox (<i>WOX</i>) transcription factors (TFs) are well known for their role in plant development but are rarely studied in citrus. In this study, we identified 11 putative genes from the sweet orange genome and divided the citrus <i>WOX</i> genes into three clades (modern/WUSCHEL(WUS), intermediate, and ancient). Subsequently, we performed syntenic relationship, intron-exon organization, motif composition, and <i>cis</i>-element analysis. Co-expression analysis based on RNA-seq and tissue-specific expression patterns revealed that <i>CsWOX</i> gene expression has multiple intrinsic functions. <i>CsWUS</i> homolog of <i>AtWUS</i> functions as a transcriptional activator and binds to specific DNA. Overexpression of <i>CsWUS</i> in tobacco revealed dramatic phenotypic changes, including malformed leaves and reduced gynoecia with no seed development. Silencing of <i>CsWUS</i> in lemon using the virus-induced gene silencing (VIGS) system implied the involvement of <i>CsWUS</i> in cells of the plant stem. In addition, CsWUS was found to interact with CsCYCD3, an ortholog in <i>Arabidopsis</i> (AtCYCD3,1). Yeast one-hybrid screening and dual luciferase activity revealed that two TFs (<i>CsRAP2.12</i> and <i>CsHB22</i>) bind to the promoter of <i>CsWUS</i> and regulate its expression. Altogether, these results extend our knowledge of the <i>WOX</i> gene family along with <i>CsWUS</i> function and provide valuable findings for future study on development regulation and comprehensive data of <i>WOX</i> members in citrus.