Acute myeloid leukemia (AML) is driven by a combination of genetic alterations and non-mutational mechanisms that disrupt normal hematopoiesis and support leukemic cell survival. While the mutational landscape of AML is well characterized, the non-genetic processes that sustain leukemic maintenance remain comparatively less understood. Here, we identify BCL2-associated transcription factor 1 (BCLAF1) as a key regulator of mRNA metabolism in AML. BCLAF1 physically associates with core spliceosome components and controls alternative splicing, with a predominant effect on intron retention. We demonstrate that BCLAF1 is required for the productive splicing of activating transcription factor 4 (ATF4) mRNA, thereby sustaining ATF4 protein expression. Loss of BCLAF1 reduces ATF4 protein levels, leading to downregulation of amino acid metabolic target genes essential for leukemic cell survival. Consistently, BCLAF1 deletion compromises ATF4 expression and impairs leukemic progression in mouse models. Moreover, analysis of patient cohort samples reveals a strong correlation between BCLAF1 and ATF4 expression. Together, these findings uncover a previously unrecognized role for BCLAF1 in coordinating mRNA splicing and metabolic adaptation in AML, highlighting its potential as a therapeutic target.