We tested grackles (Quiscalus spp.) to determine whether they retain egg rejection behavior in the absence of the selection pressure of brood parasitism. Neither Bronzed Cowbird (Molothrus aeneus) nor Brown-headed Cowbird (M. ater) parasitism was recorded in 797 Great-tailed Grackle (Q. mexicanus) nests. Cross-fostered Bronzed Cowbird nestlings, but not Brown-headed Cowbird nestlings, fledged from Great-tailed Grackle nests, indicating that Brown-headed Cowbird parasitism does not select for rejection in these grackles. Great-tailed Grackle populations sympatric and allopatric with Bronzed Cowbirds rejected 100% of model cowbird eggs. An allopatric population of Boat-tailed Grackle (Q. major), a sister species of the Great-tailed Grackle, also rejected 100% of model eggs. Egg rejection in the Boat-tailed Grackle has apparently been retained in the absence of parasitism for as long as 800,000 years since it split from the Great-tailed Grackle. The Common Grackle (Q. quiscula), which lays the most variable eggs among the grackles, also has the lowest level of egg rejection—which is consistent with the argument that it may have lost most of its rejection behavior in the absence of parasitism. With extreme intraclutch egg-variation, Common Grackles may be more likely to reject their own oddly colored eggs, which would select against rejection behavior in the absence of parasitism. Those results have significant implications for long-term parasite-host coevolution, because they suggest that egg rejection has been retained in most species of Quiscalus in the absence of parasitism. If typical of the world's avifauna, such retention may force brood parasites to specialize on a few host species and to rarely return to using old hosts, which would readily reject their eggs.