Many over-wintering plants grown in temperate climate acquire competence to flower upon prolonged cold exposure in winter, through vernalization. In Arabidopsis thaliana, prolonged cold exposure induces the silencing of the potent floral repressor FLOWERING LOCUS C (FLC) through repressive chromatin modifications by Polycomb proteins. This repression is maintained to enable flowering after return to warmth, but is reset during seed development. Here, we show that embryonic FLC reactivation occurs in two phases: resetting of cold-induced FLC silencing during embryogenesis and further FLC activation during embryo maturation. We found that the B3 transcription factor (TF) ABSCISIC ACID-INSENSITIVE 3 (ABI3) mediates both FLC resetting in embryogenesis and further activation of FLC expression in embryo maturation. ABI3 binds to the cis-acting cold memory element at FLC and recruits a scaffold protein with active chromatin modifiers to reset FLC chromatin into an active state in late embryogenesis. Moreover, in response to abscisic acid (ABA) accumulation during embryo maturation, ABI3, together with the basic leucine zipper TF ABI5, binds to an ABA-responsive cis-element to further activate FLC expression to high level. Therefore, we have uncovered the molecular circuitries underlying embryonic FLC reactivation following parental vernalization, which ensures that each generation must experience winter cold prior to flowering.