Transcripts corresponding to thousands of genes are deposited by the mother in the egg. Throughout the earliest developmental stages following fertilization, the embryo is transcriptionally silent, and these mRNA transcripts set the trajectory for subsequent development. During the maternal-zygotic transition (MZT), a substantial fraction of maternal mRNAs are targeted for degradation, and the first zygotic genes are transcribed. While some maternal and early zygotic genes have been exhaustively analyzed, the early embryonic functions of many others are unknown. The precise function of maternal mRNA degradation, and why only specific transcripts are degraded, has been debated. We created a transcriptomic dataset for 14 Drosophila species at stages before and after the maternal-zygotic transition, from single embryos, and compared our results with a previously published Aedes Aegypti developmental time course. Transcripts that that are represented at both stages are remarkably stable over evolutionary time, while the levels of transcripts that are present at only one stage vary widely between relatively close relatives. Maternally deposited genes that are degraded at the MZT vary dramatically across species, suggesting that these genes may either have an early function that is highly species-specific, or may represent developmental noise that is attenuated through degradation. While purely zygotic transcripts also vary considerably across evolutionary time, we found a small group of purely zygotic genes that are extremely conserved across hundreds of millions of years of evolution. This select group is highly enriched in transcription factors that play critical roles in early development. Our results suggest that the combined contribution of transcripts from the maternal and zygotic genomes meet the developmental constraints of the embryo, while genes expressed only from the maternal genome or zygotic genome evolve more freely.