The unfolded protein response (UPR) is activated by various stresses during vegetative development in Arabidopsis, but is constitutively active in anthers of unstressed plants. To understand the role of the UPR during reproductive development, we analyzed a double mutant, ire1a ire1b. The double mutant knocks out the RNA splicing arm of the UPR signaling pathway and is fertile at room temperature, but is male sterile at modestly elevated temperature (ET). The conditional male sterility in the mutant is a sporophytic trait, and when the double mutant was grown at ET, defects appeared in the structure of the tapetum. As a result, the tapetum in the double mutant failed to properly deposit the pollen coat at ET, which made pollen grains clump and prevented their normal dispersal. IRE1 is a dual protein kinase/ribonuclease involved in the splicing of bZIP60 mRNA, and through complementation analysis of various mutant forms of IRE1b, it was demonstrated that the ribonuclease activity of IRE1 was required for protecting male fertility from ET. It was also found that overexpression of SEC31A rescued the conditional male sterility in the double mutant. SEC31A is involved in ER to Golgi trafficking and a major target of the IRE1-mediated UPR signaling in stressed seedlings. Thus, IRE1, a major component of the UPR, plays an important role in protecting pollen development from ET.