ABSTRACT Ethylene response factors (ERFs) comprise one of the largest transcription factor families in many plant species. Tobacco (Nicotiana tabacum) ERF3 (NtERF3) and other ERF‐associated amphiphilic repression (EAR) motif‐containing ERFs are known to function as transcriptional repressors. NtERF3 and several repressor‐type ERFs induce cell death in tobacco leaves and are also associated with a defence response against tobacco mosaic virus (TMV). We investigated whether transcriptional activator‐type NtERFs function together with NtERF3 in the defence response against TMV infection by performing transient ectopic expression, together with gene expression, chromatin immunoprecipitation (ChIP) and promoter analyses. Transient overexpression of NtERF2 and NtERF4 induced cell death in tobacco leaves, albeit later than that induced by NtERF3. Fusion of the EAR motif to the C‐terminal end of NtERF2 and NtERF4 abolished their cell death‐inducing ability. The expression of NtERF2 and NtERF4 was upregulated at the early phase of N gene‐triggered hypersensitive response (HR) against TMV infection. The cell death phenotype induced by overexpression of wild‐type NtERF2 and NtERF4 was suppressed by co‐expression of an EAR motif‐deficient form of NtERF3. Furthermore, ChIP and promoter analyses suggested that NtERF2, NtERF3 and NtERF4 positively or negatively regulate the expression of NtERF3 by binding to its promoter region. Overall, our results revealed the cell death‐inducing abilities of genes encoding activator‐type NtERFs, including NtERF2 and NtERF4, suggesting that the HR‐cell death signalling via the repressor‐type NtERF3 is competitively but coordinately regulated by these NtERFs.