While the effect of natal experience on habitat and host selection has long been of interest to evolutionary biologists, the adaptive consequences of this effect have only recently been explored. The natal habitat provides dispersing individuals with information that can potentially improve estimates of three parameters that are important in sequential habitat search: habitat quality, habitat encounter rate and total time available for search. The estimates that are changed by natal experience will determine the ecological consequences of the individual variation that results from natal experience. Here, I propose methods for examining habitat acceptance during sequential search that allow discrimination between the potential effects of natal experience. I then discuss the results of an experiment using these methods to determine which habitat search parameter estimates are most influenced by natal experience in the vinegar fly, Drosophila melanogaster. I found that the natal habitat's effect on estimates of time available for search was largely responsible for differences in breeding site acceptance between individuals from different natal habitats. This type of effect is likely to be common in nature, and future tests of how natal experience influences habitat selection should take care to distinguish between this and other potential effects of natal experience.