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Actin and nuclear myosin 1 (NM1) are regulators of transcription and chromatin organization. Using a genome‐wide approach, we report here that β‐actin binds intergenic and genic regions across the mammalian genome, associated with both protein‐coding and rRNA genes. Within the rDNA, the distribution of β‐actin correlated with NM1 and the other subunits of the B‐WICH complex, WSTF and SNF2h. In β‐actin^‐/‐ mouse embryonic fibroblasts (MEFs), we found that rRNA synthesis levels decreased concomitantly with drops in RNA polymerase I (Pol I) and NM1 occupancies across the rRNA gene. Reintroduction of wild‐type β‐actin, in contrast to mutated forms with polymerization defects, efficiently rescued rRNA synthesis underscoring the direct role for a polymerization‐competent form of β‐actin in Pol I transcription. The rRNA synthesis defects in the β‐actin^‐/‐ MEFs are a consequence of epigenetic …