The N⁶-adenosine methyltransferase METTL16 regulates the expression of the SAM synthetase gene MAT2A by controlling the retention of an intron in response to intracellular levels of S-adenosylmethionine (SAM). When SAM levels are low, cells increase MAT2A expression by enhancing splicing of a retained intron. This process requires METTL16 and a conserved hairpin structure (hp1) in the 3' untranslated region (UTR) of MAT2A. METTL16 occupancy on hp1 increases under SAM-limiting conditions, promoting intron retention and splicing. METTL16 is also the methyltransferase for the U6 spliceosomal snRNA, a function conserved in yeast. These findings suggest that the conserved U6 snRNA methyltransferase evolved an additional function in vertebrates to regulate SAM homeostasis by posttranscriptionally controlling SAM synthetase gene expression. METTL16 methylates the UACAGAGAA sequence in MAT2A hairpins, which is identical to the site in U6 snRNA. METTL16 is necessary for efficient MAT2A splicing and contributes to MAT2A activity. METTL16 occupancy on hp1 promotes splicing of the retained intron, with increased dwell time on hp1 under SAM-limiting conditions. METTL16 is the long-unknown U6 snRNA methyltransferase, and its function is conserved in S. pombe. METTL16 is required for normal m⁶A methylation profiles beyond its direct effects on the methylation of U6 snRNA and MAT2A. METTL16-dependent m⁶A sites are sensitive to SAM levels, and METTL16 knockdown reduces m⁶A levels. METTL16 is a central factor in a feedback loop that links SAM levels to the expression of the SAM synthetase. METTL16 serves as both a writer and reader of m⁶A modifications. METTL16's role in splicing is mediated through its interaction with the MAT2A hairpin regions. METTL16's function in splicing is independent of its methyltransferase activity. METTL16 is required for the regulation of MAT2A splicing through its interaction with the MAT2A hairpin regions. METTL16 is the conserved U6 snRNA methyltransferase, and it has evolved an additional function in vertebrates to control SAM homeostasis by posttranscriptionally regulating SAM synthetase gene expression.The N⁶-adenosine methyltransferase METTL16 regulates the expression of the SAM synthetase gene MAT2A by controlling the retention of an intron in response to intracellular levels of S-adenosylmethionine (SAM). When SAM levels are low, cells increase MAT2A expression by enhancing splicing of a retained intron. This process requires METTL16 and a conserved hairpin structure (hp1) in the 3' untranslated region (UTR) of MAT2A. METTL16 occupancy on hp1 increases under SAM-limiting conditions, promoting intron retention and splicing. METTL16 is also the methyltransferase for the U6 spliceosomal snRNA, a function conserved in yeast. These findings suggest that the conserved U6 snRNA methyltransferase evolved an additional function in vertebrates to regulate SAM homeostasis by posttranscriptionally controlling SAM synthetase gene expression. METTL16 methylates the UACAGAGAA sequence in MAT2A hairpins, which is identical to the site in U6 snRNA. METTL16 is necessary for efficient MAT2A splicing and contributes to MAT2A activity. METTL16 occupancy on hp1 promotes splicing of the retained intron, with increased dwell time on hp1 under SAM-limiting conditions. METTL16 is the long-unknown U6 snRNA methyltransferase, and its function is conserved in S. pombe. METTL16 is required for normal m⁶A methylation profiles beyond its direct effects on the methylation of U6 snRNA and MAT2A. METTL16-dependent m⁶A sites are sensitive to SAM levels, and METTL16 knockdown reduces m⁶A levels. METTL16 is a central factor in a feedback loop that links SAM levels to the expression of the SAM synthetase. METTL16 serves as both a writer and reader of m⁶A modifications. METTL16's role in splicing is mediated through its interaction with the MAT2A hairpin regions. METTL16's function in splicing is independent of its methyltransferase activity. METTL16 is required for the regulation of MAT2A splicing through its interaction with the MAT2A hairpin regions. METTL16 is the conserved U6 snRNA methyltransferase, and it has evolved an additional function in vertebrates to control SAM homeostasis by posttranscriptionally regulating SAM synthetase gene expression.