Whole genome sequencing (WGS) has greatly improved the detection of methicillin-resistant Staphylococcus aureus (MRSA) transmission between people. We describe the transmission of two unique MRSA clones among homeless people in Copenhagen using WGS and core genome MLST (cgMLST). In 2014, an accumulation of MRSA bacteremia cases among homeless people admitted to our hospital was recognized, all having the rare MRSA spa t5147/ST88. The European Typology of Homelessness and Housing Exclusion (ETHOS) categories revealed that people who inject drugs (PWID) frequently visiting the milieu but living in private accommodation accounted for most cases. Hoping to terminate the transmission, 161 homeless people were MRSA screened in 2015, but no additional cases were found. From 2009 to 2018, 60 patients with genomically related t5147/ST88 isolates were found, of these 70% were confirmed to come from the homeless setting and 17% had bacteremia. From 2017 to 2020, cgMLST revealed a smaller MRSA outbreak including 13 PWID with a completely different clone, t1476/ST8, of which 15% had bacteremia. Our study confirms that WGS and cgMLST is excellent to reveal MRSA outbreaks. The ETHOS categorization can be useful to find the primary source of spread in the homeless community.