The basic leucine zipper (bZIP) family transcription factors play crucial roles in regulating plant development and stress response. In this study, we identified 62 ClabZIP genes from watermelon genome, which were unevenly distributed across the 11 chromosomes. These ClabZIP proteins could be classified into 13 groups based on the phylogenetic relationships, and members in the same group showed similar compositions of conserved motifs and gene structures. Transcriptome analysis revealed that a number of ClabZIP genes have important roles in the melatonin (MT) induction of cold tolerance. In addition, some ClabZIP genes were induced or repressed under red light (RL) or root-knot nematode infection according to the transcriptome data, and the expression patterns of several ClabZIP genes were further verified by quantitative real-time PCR, revealing their possible roles in RL induction of watermelon defense against nematode infection. Our results provide new insights into the functions of different ClabZIP genes in watermelon and their roles in response to cold stress and nematode infection.