Viruses reprogram host gene expression through multiple mechanisms to establish infection. Among these, RNA modifications, which are chemical marks that shape RNA fate, play key roles in viral replication and immune responses. Coronaviruses remodel host RNA modifications, such as m⁶A and m⁵C, to favor replication. However, the role of N⁷-methylguanosine (m⁷G), one of the most abundant RNA marks, in coronavirus infection remains largely unclear. Although best known as the mRNA cap modification, m⁷G is also found internally in various RNA species, including rRNA, tRNA and mRNA. Internal m⁷G has emerging roles in cancer and neurological disease, but its functions in viral infection remain unknown. Here, we report a previously unrecognized function of the coronavirus nonstructural protein 14 (NSP14) in inducing internal m⁷G on host mRNA. NSP14 converts guanosine triphosphate (GTP) to m⁷G TP via its N7-methyltransferase domain, and the resulting m⁷GTP is incorporated co-transcriptionally by RNA polymerase II, producing widespread internal m⁷G across the host transcriptome. This activity is enhanced by the viral cofactor NSP10, which occurs predominantly in the nucleus and is conserved among alpha-, beta- and gamma-coronaviruses. Functionally, NSP14-driven internal m⁷G disrupts canonical splicing programs by promoting intron retention and creating novel splice junctions, with a bias toward genes governing genome stability, RNA metabolism and nuclear processes. Pharmacological interference with internal m⁷G deposition, through the inhibition of NSP14 or RNA polymerase II, impairs SARS-CoV-2 replication, indicating that the virus hijacks the host transcriptional machinery to support infection. Together, we reveal an epitranscriptomic strategy conserved among coronaviruses that reprograms host RNA processing and identify NSP14-induced internal m⁷G as a potential antiviral target.