β-cyclocitral (βCC), a major apocarotenoid of β-carotene, enhances plants’ defense against environmental stresses. However, the knowledge of βCC’s involvement in the complex stress-signaling network is limited. Here we demonstrate how βCC reprograms the transcriptional responses that enable Solanum lycopersicum L. (tomato) plants to endure a plethora of environmental stresses. Comparative transcriptome analysis of control and βCC-treated tomato plants was done by generating RNA sequences in the BGISEQ-500 platform. The trimmed sequences were mapped on the tomato reference genome that identifies 211 protein-coding differentially expressed genes. Gene ontology and Kyoto Encyclopedia of Genes and Genomes analysis and their enrichment uncovered that only upregulated genes are attributed to the stress response. Moreover, 80% of the upregulated genes are functionally related to abiotic and biotic stresses. Co-functional analysis of stress-responsive genes revealed a network of 18 genes that code for heat shock proteins, transcription factors (TFs), and calcium-binding proteins. The upregulation of jasmonic acid (JA)-dependent TFs (MYC2, MYB44, ERFs) but not the JA biosynthetic genes is surprising. However, the upregulation of DREB3, an abscisic acid (ABA)-independent TF, validates the unaltered expression of ABA biosynthetic genes. We conclude that βCC treatment upregulates multiple stress-responsive genes without eliciting JA and ABA biosynthesis.