Although crucial for population demography, our understanding of how and to which relative extent different ecological factors constrain female reproduction suffers from difficulties in studying links between individual behavior, life history and fitness in nature. We here present such data on females in a natural population of the butterfly Leptidea sinapis. The data were combined with climate records and laboratory estimates of life history parameters to predict the relative impact of different ecological constraints on female fitness in the wild. We partitioned effects of male courtship, host plant availability, and temperature on female fitness using simulation models. Results indicate that temperature is the most constraining factor on female fitness, followed by host plant availability, whereas the short-term negative effects of male courtship detected in the field study were less important in models predicting female reproductive success over the entire lifespan. In the simulations females with more reproductive reserves were more limited by the ecological variables. Reproductive physiology and egg laying behavior were therefore predicted to be co-optimized but reach different optima for females of different body sizes, a prediction supported by the empirical data. This study thus highlights the need of studying behavioral and life history variation in orchestration to achieve a more complete picture of both demographic and evolutionary processes in naturally variable and unpredictable environments.