Abstract Combined high light and heat stress (HL+HS) causes more severe damage to the photosynthetic apparatus in plants than either high light (HL) or heat stress (HS) alone and drastically diminishes plant survival rates. Plants adapt to HL+HS stress by upregulating endogenous jasmonic acid (JA) levels. However, the pathways regulating this elevation and the signaling transduction to adapt to HL+HS remain unknown. Here, we identified the key gene sulfotransferase 2A (SlST2A) involved in JA metabolism and the upstream transcription factor heat shock factor B2b (SlHSFB2b) through transcriptome analysis and biochemical experiments. Under HL+HS conditions, SlHSFB2b expression was enhanced in tomato (Solanum lycopersicum); this suppressed SlST2A transcription, inhibiting JA catabolism and promoting the accumulation of endogenous JA. The elevated JA activated a transcriptional cascade orchestrated by SlMYC2, regulating transcription factors SlZF2 and SlDREB2A as well as functional genes such as SlSAP7, SlBAG2, and SlPDX1.2, thereby enhancing tomato tolerance to HL+HS. Our findings provide insights into the mechanistic basis of endogenous JA upregulation and the complex response network mediated by JA under combined HL+HS stress in plants.