Potato (Solanum tuberosum L.) is a modified stem and important food crop rich in starch, proteins, antioxidants, and vitamins. Potato is consumed globally; however, being a temperate region crop, it is negatively affected by temperature rise. Histone methylation dynamically regulates plant growth and development in response to environmental stresses. It is a reversible process mediated by distinct histone methyltransferases and histone demethylases, resulting in the modification of chromatin structure to activate or repress transcription. The JmjC domain-containing histone demethylase proteins are involved in histone demethylation, sustaining homeostasis of histone methylation levels. However, the potato JMJ gene family histone demethylases remain uncharacterized and their expression dynamics under heat stress are unknown. In this study, genome-wide analysis led to the identification of a total of 26 StJMJ proteins in potato, which were classified based on their conserved motifs, domains, and gene structure. Phylogenetic analysis categorized StJMJ gene family into five classes, named as KDM5/JARID1, KDM4/JHDM3, KDM3/JHDM2, JMJD6, and JmjC-only. In silico sub-cellular localization studies showed that StJMJ family members were uniformly distributed among various sub-cellular compartments. Promoter analysis revealed the presence of cis-regulatory elements involved in light, development, hormones, and stress responses. Furthermore, gene expression profiling of StJMJs in leaf and stolon tissues of heat-sensitive (HS) and heat-tolerant (HT) genotypes under elevated temperature was performed. The expression of StJMJ3, StJMJ6, StJMJ8, StJMJ10, StJMJ12, StJMJ15, StJMJ16, StJMJ17, StJMJ18, StJMJ19, and StJMJ21 were heat inducible in the leaf tissue of both genotypes, while showed antagonistic expression (upregulated in HS, downregulated in HT) in stolon tissue. Additionally, StJMJ11 was found to be significantly upregulated in the leaf and stolon of both genotypes. Collectively, this study hints towards the role of StJMJ genes as important epigenetic regulators modulating heat tolerance in potato.