WRKY transcription factors (TFs) play significant roles in plant development. However, they have not yet been studied in terms of the impact they have on the common fig (Ficus carica L.), a significant fruit species in Mediterranean countries. In this study, we extensively examined the full-genome F. carica WRKY (FcWRKYs) gene complement (47 genes), in terms of gene structure, protein domains and motifs, physicochemical properties, phylogenetic relationships and selection pressure. Based on the structural properties of the encoded proteins, we grouped the FcWRKY genes into three main groups (I, II and III), with the second group being further divided into five subgroups (a–e). Subgroup IId FcWRKY proteins were discovered to contain the Plant zinc cluster (Plant-zn-clust) domain and Ca²⁺-dependent Calmodulin (CaM)-binding domain (CaMBD). In total, we discovered ten conserved motifs, seven of which may be associated with WRKY functional specificities attributable to a single group or a small number of groups. Phylogenetically related members shared similar exon–intron structure, with the average number of exons being higher (~ 5) in (sub)groups I, IIa, IIb compared to IIc, IId, IIe and III (~ 3). Comparative phylogeny using the mulberry WRKY gene complement (MnWRKYs) revealed 38 pairs of orthologous genes shared by both species, which diverged from 84.3 to 25.3 million years ago (Mya) and have been evolving under purifying selection that was weaker on group III genes, suggesting an important role of this group in the enlargement of the adaptive array of WRKY TFs. RNA-seq results revealed that genes that were highly expressed in the peel across all fruit developmental stages belonged to group I and subgroups IIb, IIc, IId and IIe, suggesting the role played by these members in fruit peel development. RT-qPCR validated this profile and further showed that three genes FcWRKY25 (IIc), FcWRKY31 (IIb), and FcWRKY39 (IIc) are clearly more overexpressed during color acquisition in the Tunisian dark cultivar ‘Zidi’, in comparison with the light purple cultivar ‘Soltani’, presenting these three genes as potential contributors to the changes in biochemical compounds in the fig peel during fruit maturation. The knowledge framework provided by our study will be a valuable asset in the functional exploration of candidate genes that may be associated with fruit quality.