Lily bulbils, which serve as advantageous axillary organs for vegetative propagation, have not been extensively studied in terms of the mechanism of bulbil initiation. The function of auxin and sucrose metabolism have been implicated in axillary organ development, but their relationship in regulating bulbil initiation remains unclear. In this study, exogenous indole-3-acetic acid (IAA) treatment increased the endogenous auxin levels at leaf axils and significantly decreased bulbil number, whereas treatment with the auxin polar transport inhibitor N-1-naphthylphthalamic acid (NPA), which resulted in a low auxin concentration at leaf axils, stimulated bulbil initiation and increased bulbil number. A low level of auxin caused by NPA spraying or silencing of auxin biosynthesis genes YUCCA FLAVIN MONOOXYGENASE-LIKE6 (LlYUC6) and TRYPTOPHAN AMINO-TRANSFERASE1 (LlTAR1) facilitated sucrose metabolism by activating the expression of LlSusy1 and LlCWIN2, resulting in enhanced bulbil initiation. Silencing SUCROSE SYNTHASES1 (LlSusy1) or CELL WALL INVERTASE2 (LlCWIN2) hindered bulbil initiation. Moreover, the transcription factor BASIC-HELIX-LOOP-HELIX35 (LlbHLH35) directly bound the promoter of LlSusy1, but not the promotor of LlCWIN2, and activated its transcription in response to the auxin content, bridging the gap between auxin and sucrose metabolism. In conclusion, our results reveal a LlbHLH35-LlSusy1 module mediates auxin-regulated sucrose metabolism during bulbil initiation.