Autophagy has been reported to regulate many different cellular processes. However, numerous reports develop contrasting models and opposite roles for autophagic functions. For example, autophagy was shown to have opposite functions in mammalian cells during reprogramming into pluripotency (Wang et al., 2013 Cell Stem Cell 13, 617 vs. Wu et al., 2015 Nat Cell Biol 6, 715) and in immune related cell death in plants (Liu et al., 2005, Cell 121, 567 vs. Hofius et al., 2009, Cell 137, 773). Using a variety of mechanistic approaches, we provide a new conceptual template that would reconcile these discrepancies, and further highlight the importance of autophagy in cellular reprogramming and organismal fitness. We find that autophagy functions as an intrinsic component in temporary reprograming to attenuate current cellular states and to allow new programs to unfold while controlling their intensity. Accordingly, autophagic dysfunction leads to defects in organismal fitness and de-differentiation of somatic cells into pluripotency.