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Monarch butterflies are best known from their migratory North American range, although many resident, year-round breeding populations are established throughout the world. Here, we evaluate two non-exclusive hypotheses for the loss of migration in resident monarch populations: (1) absence of cues that trigger migration; and (2) loss of sensory, neural or physiological systems required for migration. To evaluate the first hypothesis, we exposed resident monarchs from Queensland, Australia to decreasing larval photoperiod and observed reproductive development in resulting females to assess their propensity to show reduced reproductive development, a precursor for long-distance migration. To address the second hypothesis, we measured antennal circadian clock gene expression, a crucial element of the monarch's ability to orientate directionally, in a resident and a migratory population. We found that Australian resident monarchs show reduced reproductive development in response to decreasing photoperiod, consistent with the 'loss of cues' hypothesis. We found no differences in antennal clock gene expression between migratory and resident populations, inconsistent with the 'loss of mechanism' hypothesis. Together, these data indicate that even after hundreds of generations of non-migration, monarchs retain two crucial elements of their migratory repertoire: developmental plasticity associated with decreasing photoperiod and antennal circadian rhythms necessary for directional orientation.