The museum's origins reach back to 1697, when Robert Sibbald presented the University of Edinburgh's College of Medicine with a natural history collection assembled with his friend Andrew Balfour. Daniel Defoe visited and called it a fine Museum, or Chamber of Rarities, which in some things was not to be matched in Europe. Later editions of his book said it had rarities not found in the Royal Society or the Ashmolean Museum. The collection grew under Robert Jameson, who took charge in 1804 and transformed it from a university department into something approaching a national institution. Half of all specimens collected by Royal Navy survey ships were sent to Edinburgh, the other half to the British Museum. The taxidermist John Edmonstone worked at the museum, and in 1826 gave private lessons to a young Charles Darwin.

The museum's Victorian building began with ceremony and ended with tragedy. On 23 October 1861, Prince Albert laid the foundation stone. It was his last public appearance before his death six weeks later. The architect Francis Fowke designed a grand central hall of cast iron construction with a Victorian Venetian Renaissance facade that rises the full height of the building. Construction proceeded in phases -- the eastern sections opened in 1866, while the western wing was not completed until 1888. A corridor linking the museum to the university was nicknamed the Bridge of Sighs. Students once found refreshments stored there for an official reception and consumed the lot, leaving nothing for the Edinburgh worthies the drinks were intended for. A door was promptly installed.

Today the museum is two buildings fused together on Chambers Street. The Victorian building, restored and reopened in 2011 after a three-year, 47-million-pound renovation, contains galleries covering natural history, world cultures, European art and design, and science and technology. The Grand Gallery holds a display called the Window on the World, rising through four storeys and containing over 800 objects. Adjacent to it stands the Museum of Scotland, a modern building opened in 1998 and clad in golden Moray sandstone, housing Scottish history and archaeology in a chronological arrangement from prehistory upward. The two institutions merged in 2006, dropping the word Royal to create a unified brand after years of confusing visitors with separate names.

The collection spans the breadth of human history. Eleven of the Lewis chessmen -- the 12th-century gaming pieces carved from walrus ivory -- sit in Edinburgh, while their companions reside in the British Museum. The Hunterston Brooch, dating to around 700 AD, and the Monymusk Reliquary, an 8th-century casket said to have been carried at Bannockburn, are among the oldest Scottish artifacts on display. The Scottish Maiden, the beheading machine used in Edinburgh from the 16th to the 18th century, remains a favorite with visiting schoolchildren. In 2022, the museum agreed to return the Ni'isjoohl totem pole to the Nisga'a people of British Columbia, completing its repatriation in September 2023. The 36-foot pole was carved in 1855 and arrived in Scotland in 1930 after being taken without consent. Its return represents a broader reckoning with how museum collections were assembled.