Fungi produce large quantities of clonal asexual spores, which are highly resistant entities that can stay dormant for a long time until favorable conditions are encountered. How fungal spores prepare for dormancy is not known. Studies have shown that spores contain abundant stable messenger RNAs (mRNAs); however, their origin and purpose remain unclear. Our work showed that the so-called dormant conidia of three filamentous fungal species (Aspergillus nidulans, Aspergillus fumigatus and Talaromyces marneffei) have robust transcription activities to synthesize their own mRNAs. Conidia remain transcriptionally active and responsive to the changing environment (i.e., not dormant) until they leave the developmental structure. Environment-specific transcriptional responses can influence conidial content, expedite gene expression when dormancy is broken, and affect the subsequent fitness and capabilities of the fungal cells after germination, including drug and stress resistance, mycotoxin and secondary metabolite production, and virulence. Our findings uncover a mechanism for how genetically identical conidia achieve phenotypic variation and suggest that conidia prepare for the future by synthesizing and storing transcripts according to their experience before entering dormancy.