The colonization of an introduced plant by soapberry bugs in Florida has resulted in the rapid evolution of a distinctive “host race.” Differences in the synchrony and persistence of local seed crops may have favored interracial differentiation in flight/life history tactics. To advance previous work, we quantified seed availability in individual native and introduced host plants. We tested the prediction that the new host’s relatively discrete period of annual seed production has selected for a higher frequency of a short-winged, flightless morph with a briefer generation time. Contrary to that prediction, short-winged bugs were not more common in the derived race, but further investigation revealed the unexpected presence of a long-winged morph, that like the short-winged, lacks flight muscle and exhibits the same rapid life cycle advantages. Consistent with prediction, the derived race, descended from volant long-winged colonists, shows an abundance of this “cryptic” flightless morph. In total, four flight/life history morphs were discovered, including two additional long-winged types that either histolyze or retain flight muscle. The morphs differed in life history traits both within and between host races. Morph frequency may be influenced by evolution in correlated characters: we found that beak length, which has rapidly evolved to be shorter on the smaller fruits of the introduced host, is discontinuously distributed between flight morphs, being greater in long-winged bugs. This study shows complex, unpredicted evolutionary relations between a mobility character, a trophic character, and the life history.