Dark septate endophytes (DSEs) are one of the most studied groups of root fungal endophytes in recent years. However, the effects of DSE on host plant are still under debate, and the molecular mechanisms are poorly understood. In this study, we identified a DSE fungus of the genus Anteaglonium, named T010, from the wild blueberry. When inoculated into Vaccinium corymbosum L. plants, T010 could enhance root growth and promote shoot branching, leading to increased plant growth. By comparative transcriptome analysis, we obtained 1948 regulated differentially expressed genes (DEGs) from the V. corymbosum plants treated by T010. Further functional enrichment analysis identified a series of DEGs enriched in transcriptional regulation, material transport, phytohormone biosynthesis and flavonoid biosynthesis. Moreover, the comparative analysis of liquid chromatography–mass spectrometry verified that T010 treatment induced the changes in the contents of various phytohormones and flavonoids. This is the first report on the isolation of DSE fungi of the genus Anteaglonium from blueberry roots. Moreover, our results suggested that T010 colonization could result in a series of changes in cell metabolism, biosynthesis and signal pathways, thereby promoting plant growth. Particularly, the changes of phytohormone and flavonoid metabolism induced by T010 colonization might contribute to the promotion of blueberry growth. Our results will provide new insights into understanding of the interaction of DSE fungi and host plants, as well as the development and utilization of DSE preparations.