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To \u201cunmask\u201d and study how innate immune inhibition affects cell type-specific transcriptional regulation of the human and viral genome, we performed single-cell RNA sequencing of human brain cell co-cultures, comparing an isolate of rabies virus (RABV) to its mutant incapable of antagonizing interferon- and NF-\u03baB-dependent responses. RABV gene expression was shaped by host cell type. RABV induced small-scale, cell-type conserved transcriptional programs that likely support infection by 1) hijacking negative transcriptional feedback of pro-viral factors while 2) reducing anti-viral RNAs. Unexpectedly, disinhibited innate immune signaling increased RABV transcription, most strikingly in an infection-independent \u201cpro-viral\u201d astrocyte subpopulation. 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