The emergence of life-threatening methicillin-resistant Staphylococcus aureus (MRSA) has led to increased interest in the use of bacteriophages as an alternative therapy to antibiotics. The success of phage therapy is greatly dependent on the selected phage possessing a wide host range. This study describes phage MR003 isolated from sewage influent at a municipal wastewater treatment plant in Tokyo, Japan. MR003 could infect 97% of 104 healthcare- and community-associated MRSA strains tested, compared with 73% for phage SA012, which has a broad host range against bovine mastitis S. aureus. Genome analysis revealed that MR003 belongs to the genus Silviavirus which has not been studied extensively. MR003 recognizes and binds to wall teichoic acid (WTA) of S. aureus during infection. In silico comparisons of the genomes of MR003 and SA012 revealed that ORF117 and ORF119 of MR003 are homologous to the putative receptor-binding proteins ORF103 and ORF105 of SA012, with amino acid similarities of 75% and 72%, respectively. ORF104, which is an N-acetylglucosaminidase found in the MR003 tail, may facilitate phage's infection onto the WTA-null S. aureus RN4220. The differences in tail and baseplate proteins may be key contributing factors to the different host specificities of MR003 and SA012. MR003 showed strong adsorptivity, but not infectivity, against S. aureus SA003, which may be influenced by the bacterium's restriction modification system. This study expands our knowledge of the genomic diversity and host specificity of Silviavirus, which is a potential phage therapy candidate for MRSA infections.