Floral resources and natural enemies are considered important drivers of wild bee population dynamics, yet there is little information on how these factors, either independently or in combination, influence the demographic performance of bees. Bumble bees (Bombus spp.), ecologically important social insects, have long colony cycles lasting many weeks. Food shortfalls during the colony lifetime can result in smaller colony sizes and lower reproductive output. Conopid flies (Conopidae, Diptera) are prevalent endoparasitoids of bumble bees, often infecting high percentages of free‐flying individuals. Conopids can reduce worker life span and foraging efficiency; consequently, they may negatively affect colony success. In this study, we evaluated how seasonal variability in food resources and conopid parasitism together influence the productivity of bumble bee colonies through construction of a simulation model. In addition to simulating colony performance in relation to a defined food environment and conopid‐induced worker mortality, we evaluated how daily background mortality risk and the timing of colony initiation affected growth and reproductive outcomes of colonies, as well as the degree of influence exerted by conopids. Model parameters were largely informed by field data collected from Bombus impatiens colonies at our study site (Blandy Experimental Farm, Boyce, Virginia, USA), including data on forager risk of conopid parasitism as assessed using radio‐frequency identification (RFID) technology. In spite of the high probability of parasitism (4% per hour of flight during seasonal peak) incorporated into our model simulations, lethal parasitism by conopids generally had a modest influence on colony productivity, reducing reproductive output by 15% or less across most tested scenarios. However, conopids were more influential under very low resource conditions, reducing reproductive output by 21–28%. Inclusion of sublethal effects of conopids on foraging activity further reduced colony performance in all scenarios, but had a greater impact on colony performance under the poorest resource conditions. This work emphasizes that the importance of natural enemies to the demographic performance of bees can increase under certain environmental conditions and highlights the value of using models to consider multiple stressors that are difficult to evaluate simultaneously in field experiments.