In eukaryotes, most RNA molecules are exported into the cytoplasm after transcription. Long noncoding RNAs (lncRNAs) reside and function primarily inside the nucleus, but nuclear localization of mRNAs has been considered rare in both animals and plants. Here we show that Arabidopsis anaphase-promoting complex/cyclosome (APC/C) coactivator genes CDC20 and CCS52B (CDH1 ortholog) are co-expressed with their target cyclin B genes (CYCBs) during mitosis. CYCB transcripts can be exported and translated; however, CDC20 and CCS52B mRNAs are confined to the nucleus at prophase, and the cognate proteins are not translated until the redistribution of the mRNAs to the cytoplasm after nuclear envelope breakdown (NEBD) at prometaphase. The 5' untranslated region (UTR) plays dual roles in CDC20 mRNA nuclear localization and translation. Mitotic accumulation of CDC20 and CCS52B transcripts enables the timely and rapid activation of APC/C, while the nuclear sequestration of these transcripts at prophase appears to protect cyclins from precocious degradation.