Transcription by RNA polymerase II (Pol II) is a tightly regulated process in eukaryotes. A recent study revealed that the trimethylation of histone H3 at lysine 4 (H3K4me3) activates gene expression by promoting Pol II pause-release and transcription elongation rather than transcription initiation. However, the molecular mechanisms linking H3K4me3 to transcription elongation remain largely unclear. Here, we show that an H3K4me3 reader recruits the positive transcription elongation factor B (P-TEFb) complex to regulate this process. Genetic screenings in Arabidopsis reveal that RGSA1 is required for the expression of genes induced by the plant hormone salicylic acid. RGSA1 encodes an H3K4me3 reader containing a cysteine-tryptophan domain critical for its function. RGSA1 mainly occupies transcription start sites, where it recruits P-TEFb to promote the release of paused Pol II and facilitate transcription elongation. Given the evolutionary conservation of H3K4me3 readers and P-TEFb, our findings may represent a conserved mechanism underlying transcription elongation across eukaryotes.