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Anopheles gambiae and its sibling species Anopheles coluzzii are the most efficient vectors of the malaria parasite Plasmodium falciparum. When females of these species feed on an infected human host, oogenesis and parasite development proceed concurrently, but interactions between these processes are not fully understood. Using multiple natural P. falciparum isolates from Burkina Faso, we show that in both vectors, impairing steroid hormone signaling to disrupt oogenesis leads to accelerated oocyst growth and in a manner that appears to depend on both parasite and mosquito genotype. Consistently, we find that egg numbers are negatively linked to oocyst size, a metric for the rate of oocyst development. Oocyst growth rates are also strongly accelerated in females that are in a pre-gravid state, i.e. that fail to develop eggs after an initial blood meal. Overall, these findings advance our understanding of mosquito-parasite interactions that influence P. falciparum development in malaria-endemic regions. Author summary: Malaria, an infectious disease caused by Plasmodium parasites, continues to affect millions of people each year. These parasites are transmitted by Anopheles mosquitoes during blood feeding, which is required by females to produce eggs. After they are ingested by the female, parasites start developing in the midgut at the same time as the mosquito initiates oogenesis, the process of egg development. Here, we investigated how the concomitant processes of egg and parasite development interact in field-derived Anopheles and Plasmodium isolates. We found that in these naturally occurring pairs, oogenesis is negatively linked to parasite development, such that mosquitoes producing fewer eggs harbor faster growing oocysts. Furthermore, when we disrupt signaling pathways that drive oogenesis, oocyst growth is accelerated in a manner that appears to depend on both mosquito and parasite genotype. Additionally, when field mosquitoes fail to develop eggs, they are likely to have faster growing oocysts. The interaction between key mosquito and parasite developmental processes revealed here underscores how intimately linked Plasmodium are to mosquito physiology and can help inform the development of future vector control tools that are both safe and effective. [ABSTRACT FROM AUTHOR]