Circular RNAs (CircRNAs) regulate plant growth and development; however, their role in poplar heterosis is unclear. We identified 3722 circRNAs in poplar leaves, most of which were intergenic (57.2%) and exonic (40.2%). The expression of circRNAs in F1 hybrids with high growth potential was higher than that in those with low growth potential. Non-additive expression of circRNAs and single-parent expression of circRNAs (SPE-circRNAs) might regulate poplar heterosis through microRNA sponging and protein translation, respectively. DECs among F1 hybrids with different growth potentials might regulate the growth potential of poplar via microRNA sponging. Correlation analysis between circRNA expression and its parent gene expression showed that SPE-M circRNA (circRNAs expressed by male parent only) might regulate poplar heterosis by inhibiting parent gene expression, while other circRNAs might regulate poplar heterosis by enhancing parent gene expression. Weighted correlation network analysis of gene/circRNA expression showed that circRNAs mainly regulate poplar heterosis via carbohydrate metabolism, amino acid metabolism, energy metabolism, and material transport. In addition, we identified seven circRNAs that positively or negatively regulate poplar heterosis. Thus, non-additively expressed circRNAs and SPE circRNAs are involved in regulating poplar heterosis, and DECs among F1 hybrids with different growth potentials were involved in regulating poplar growth potential.