Coronaviruses (CoVs) pose a persistent threat to human health; however, key knowledge gaps remain in our understanding of their virus-host interactions. Prior studies identified a regulatory role for N6-methyladenosine (m6A) RNA modification in human CoV infection. M6A influences critical aspects of cellular mRNA metabolism, such as splicing, stability, export and translation and is installed by the methyltransferase, METTL3, co-transcriptionally. Our research demonstrated that small-molecule inhibition of METTL3 reduces replication and gene expression of pandemic SARS-CoV-2 and seasonal human β-coronavirus OC43, highlighting its potential as an antiviral strategy. However, the mechanism of this restriction remains unclear. Using OC43, we examined whether impaired viral replication results from dysregulation of host dependency factors, host anti-viral responses, or dependence on viral RNA modification. Functional interrogation of innate immune sensors of viral RNA and inflammatory gene expression revealed that the pro-viral role of METTL3 was not dependent on host antiviral responses. Deficits in viral RNA accumulation were detected within 5 hours of METTL3 inhibition, and when host RNA transcription was inhibited, rendering host dependency factor dysregulation an unlikely mechanism. Using a novel coronavirus RNA decay assay, we observed that METTL3 inhibition does not destabilise viral RNA. Instead, we observed impaired production of double-stranded RNA (dsRNA), a crucial intermediate formed during CoV replication, consistent with a requirement for m6A modification of viral RNA for positive and negative sense viral RNA synthesis.