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The anti-MERS-CoV activities of three medicinal plants (<i>Azadirachta indica</i>, <i>Artemisia judaica</i>, and <i>Sophora tomentosa</i>) were evaluated. The highest viral inhibition percentage (96%) was recorded for <i>S. tomentosa</i>. Moreover, the mode of action for both <i>S. tomentosa</i> and <i>A. judaica</i> showed 99.5% and 92% inhibition, respectively, with virucidal as the main mode of action. Furthermore, the anti-MERS-CoV and anti-SARS-CoV-2 activities of <i>S. tomentosa</i> were measured. Notably, the anti-SARS-CoV-2 activity of <i>S. tomentosa</i> was very high (100%) and anti-MERS-CoV inhibition was slightly lower (96%). Therefore, the phytochemical investigation of the very promising <i>S. tomentosa</i> L. led to the isolation and structural identification of nine compounds (<b>1</b>–<b>9</b>). Then, both the CC₅₀ and IC₅₀ values for the isolated compounds against SARS-CoV-2 were measured. Compound <b>4</b> (genistein 4’-methyl ether) achieved superior anti-SARS-CoV-2 activity with an IC₅₀ value of 2.13 µm. Interestingly, the mode of action of <i>S. tomentosa</i> against SARS-CoV-2 showed that both virucidal and adsorption mechanisms were very effective. Additionally, the IC₅₀ values of <i>S. tomentosa</i> against SARS-CoV-2 and MERS-CoV were found to be 1.01 and 3.11 µg/mL, respectively. In addition, all the isolated compounds were subjected to two separate molecular docking studies against the spike (S) and main protease (M^pr°) receptors of SARS-CoV-2.