Marine water temperatures are increasing due to anthropogenic climate change, constituting a major threat to marine ecosystems. Diatoms are major marine primary producers, and as such, they are subjected to marine heat waves and rising ocean temperatures. Additionally, under low tide, diatoms are regularly exposed to high temperatures. However, physiological and epigenetic responses to long-term exposure to heat stress remain largely unknown in the diatom Phaeodactylum tricornutum. In this study, we investigated changes in cell morphology, photosynthesis, and H3K27me3 abundance (an epigenetic mark consisting of the tri-methylation of lysine 27 on histone H3) after moderate and elevated heat stresses. Mutants impaired in PtEZH—the enzyme depositing H3K27me3—presented reduced growth and moderate changes in their PSII quantum capacities. We observed shape changes for the three morphotypes of P. tricornutum (fusiform, oval, and triradiate) in response to heat stress. These changes were found to be under the control of PtEZH. Additionally, both moderate and elevated heat stresses modulated the expression of genes encoding proteins involved in photosynthesis. Finally, heat stress elicited a reduction of genome-wide H3K27me3 levels in the various morphotypes. Hence, we provided direct evidence of epigenetic control of the H3K27me3 mark in the responses of Phaeodactylum tricornutum to heat stress.