Although acute myeloid leukemia (AML) with the RUNX1::RUNX1T1 fusion [t(8;21)(q22;q22.1)] defines a distinct cytogenetic subtype, differences in treatment response suggest additional molecular contributors beyond chromosomal abnormalities. Long non-coding RNAs (lncRNAs) regulate haematopoiesis and leukemogenesis. To investigate their role in t(8;21) AML, we performed whole-transcriptome sequencing of pediatric patients and age-matched healthy controls, identifying significant downregulation of lncRNA HOTAIRM1, a regulator of myeloid differentiation (adjusted P < 0.05). This was confirmed in three datasets: single-cell RNA-sequencing (GSE116256), the Leukemia MILE study (GSE13159, P=0.03), and the current study (P<0.0001). Analysis of downstream pathways activated by HOTAIRM1 loss identified miR-222, an oncomiR, as a de-repressed target (P=0.01). Elevated miR-222 expression was observed across AML cell lines (P<0.05), leukemic stem and progenitor cells (GSE117090, P<0.05), AML plasma-derived exosomes (GSE142699, P<0.0001), the current study dataset (P<0.0001), and the TARGET AML dataset (P<0.0001). Restoring HOTAIRM1 expression with epigenetic agents azacytidine and panobinostat induced apoptosis in venetoclax-resistant Kasumi-1 cells (P<0.01), through suppression of miR-222 (P<0.01) and downregulation of anti-apoptotic proteins BCL-xL and MCL-1 (P<0.05), key mediators of the venetoclax resistance mechanism. Machine learning based feature selection and Cox regression analysis showed that high miR-222 expression predicts poor outcome in pediatric t(8;21) AML, validated in both our institutional pediatric AML cohort (P<0.05) and the multi-institutional TARGET cohort (P<0.0001). Together, our findings highlight an epigenetic based approach to restore HOTAIRM1 pathway function in venetoclax-resistant AML cells, and identify miR-222 as a prognostic marker to refine risk stratification within the traditionally favorable-risk t(8;21) AML subgroup.