Sporulation of Saccharomyces cerevisiae is a developmental process in which four haploid spores are created within a single mother cell. During this process, the prospore membrane is generated de novo on the spindle pole body, elongates along the nuclear envelope and engulfs the nucleus. By screening previously identified sporulation-defective mutants, we identified additional genes required for prospore membrane formation. Deletion of either ERV14, which encodes a COPII cargo receptor, or the meiotically induced SMA2 gene resulted in misshapen prospore membranes. Sma2p is a predicted integral membrane that localized to the prospore membrane in wild-type cells but was retained in the ER in erv14 cells, suggesting that the prospore membrane morphology defect of erv14 cells is due to mislocalization of Sma2p. Overexpression of the ERV14 paralog ERV15 largely suppressed the sporulation defect in erv14 cells. Although deletion of ERV15 alone had no phenotype, erv14 erv15 double mutants displayed a complete block of prospore membrane formation. Plasma membrane proteins, including the t-SNARE Sso1p, accumulated in the ER upon transfer of the double mutant cells to sporulation medium. These results reveal a developmentally regulated change in the requirements for ER export in S. cerevisiae.