In the present work, we study the genetic control of reproductive traits under different heat stress conditions in two populations of inbred lines derived from crosses between two S. pimpinellifolium accessions and two tomato cultivars (E9×L5 and E6203×LA1589). The temperature increase affected the reproductive traits, especially at extremely high temperatures, where only a few lines were able to set fruits. Even though a relative modest number of QTLs was identified, two clusters of QTLs involved in the responses of reproductive traits to heat stress were detected in both populations on chromosomes 1 and 2. Interestingly, several epistatic interactions were detected in the E9×L5 population, which were classified into three classes based on the allelic interaction: dominant (one locus suppressed the allelic effects of a second locus), co-adaptive (the double-homozygous alleles from the same parent alleles showed a higher phenotypic value than the combination of homozygous alleles from alternative parents) and transgressive (the combination of double-homozygous alleles from different parents showed better performance than double-homozygous alleles from the same parents). These results reinforce the important role of non-additive genetic variance in the response to heat stress and the potential of the new allelic combinations that arise after wide crosses.