Heat stress, caused by elevated temperatures, is a major environmental factor limiting crop plants` productivity, thus presenting a food security challenge. Various approaches are therefore taken to develop crop species with enhanced tolerance to heat stress conditions. Since epigenetic mechanisms play an important regulatory role in mediating plants’ responses to the environment, we aim to understand the involvement of DNA methylation in the response to heat stress conditions, using tomato (Solanum lycopersicum), an important vegetable crop, as a model. We found that the tomato ddm1b mutant, impaired in DNA methylation patterns due to the downregulation of the DDM1b (DECREASE in DNA METHYLATION 1b) gene, displays improved reproductive performance under heat stress conditions. Transcriptional and DNA methylation analyses revealed that a single heat stress responsive transcription factor – HsfC1, is transcriptionally induced in the ddm1b mutant, accompanied by reduced CG and CHG methylation levels in its promoter region. These results suggest that HsfC1 is a central factor underlying the heat stress tolerance phenotype of the ddm1b mutant, linking DNA methylation with plants` response to heat stress.