Synovigenic insects (i.e., insects emerging with few ripe eggs and maturing more eggs during the course of their lifetime) may suffer from transient egg limitation due to the stochastic nature of encounters with patchy hosts and the low availability of ripe eggs at any given time point. Egg limitation also affects the stability of host–parasitoid models. Thus, quantification of the behavioral decisions influencing egg maturation, identification of the underlying physiological mechanisms, and determination of the rate of egg maturation are highly relevant to both parasitoid behavioral ecology and host–parasitoid population dynamics. The aim of this study was to identify, in a highly controlled setting, the physiological processes responsible for egg manufacture after varying host use by a synovigenic parasitoid. We quantified the time course of the reproductive hormonal response and subsequent egg production in the host feeding bruchid parasitoid, Eupelmus vuilleti (Hymenoptera: Eupelmidae) for three treatments: (1) host examination without further host use, (2) host feeding, and (3) host feeding followed by oviposition. We carried out continuous behavioral observations with single hosts, enzyme immunoassays for quantifying ecdysteroids, and ovary dissection. Ecdysone levels increased within two minutes of contact with a host, the fastest hormonal response reported for any insect. Even simple contact with a host, without further host use, triggered an increase in hormone levels, leading to the maturation of a single egg, using body reserves only. Feeding on the host caused a much larger increase in ecdysone levels and was followed by a marked increase in oogenesis. Oviposition had a weak effect on hormone levels, but increased oogenesis. We discuss the mechanisms responsible for these rapid responses, the source of ecdysteroids, and the implications of our results for the population dynamics of host–parasitoid systems and the behavioral ecology of synovigenic species.