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The <i>B-box</i> (<i>BBX</i>) gene family includes zinc finger protein transcription factors that regulate a multitude of physiological and developmental processes in plants. While <i>BBX</i> gene families have been previously determined in various plants, the members and roles of peanut <i>BBXs</i> are largely unknown. In this research, on the basis of the genome-wide identification of <i>BBXs</i> in three peanut species (<i>Arachis hypogaea</i>, <i>A. duranensis</i>, and <i>A. ipaensis</i>), we investigated the expression profile of the <i>BBXs</i> in various tissues and in response to salt and drought stresses and selected <i>AhBBX6</i> for functional characterization. We identified a total of 77 <i>BBXs</i> in peanuts, which could be grouped into five subfamilies, with the genes from the same branch of the same subgroup having comparable exon–intron structures. In addition, a significant number of <i>cis</i>-regulatory elements involved in the regulation of responses to light and hormones and abiotic stresses were found in the promoter region of peanut <i>BBXs</i>. Based on the analysis of transcriptome data and qRT-PCR, we identified <i>AhBBX6</i>, <i>AhBBX11</i>, <i>AhBBX13</i>, and <i>AhBBX38</i> as potential genes associated with tolerance to salt and drought. Silencing <i>AhBBX6</i> using virus-induced gene silencing compromised the tolerance of peanut plants to salt and drought stresses. The results of this study provide knowledge on peanut <i>BBXs</i> and establish a foundation for future research into their functional roles in peanut development and stress response.