The Joanneum was founded in 1811 by Archduke Johann together with the Styrian estates as the "Innerösterreichisches Nationalmuseum" ("Inner Austrian National Museum"). In its early years it was above all a combination of teaching and research institute and a museum focusing on scientific and technical objects. Renowned scientists worked there, including Friedrich Mohs, who developed a mineral hardness scale named after him in Graz. During the nineteenth century, the University of Technology in Graz and the Montanuniversität Leoben (Mining University of Leoben) developed from the Joanneum. Through the archduke's endowment instruction to collect and reflect the history of the province in a single location, more and more works of historical, artistic and cultural value were acquired. At the same time the Grazer Zeichenakademie (Graz Drawing Academy), founded in 1785, established the Landesbildergalerie (Styrian Painting Gallery), which was incorporated in the Joanneum during the nineteenth century. A reading group was founded, which in the twentieth century became the Steiermärkische Landesbibliothek (Styrian Provincial Library). The Joanneum archive ultimately became the Steiermärkisches Landesarchiv. Following the separation of the museum from the technical university in 1887, the collections were merged to form the Landesmuseum Joanneum with eleven separate departments: four scientific collections, five art and cultural history departments, a library and an archive. Through the acquisition of further buildings (Landeszeughaus 1892, Museumsgebäude Paulustorgasse – Volkskundemuseum 1913) and a major new building in Neutorgasse (1895), the institute grew to become the largest provincial museum in Austria.

Until a director was appointed for the first time in 1936, the Joanneum was headed by a committee with seven or eight members, the "Kuratorium". After the annexation of Austria in 1938, however, the first director Eduard Coudenhove-Erthal (1890–1964) was forced to resign following the restructuring of the Joanneum at the instigation of Josef Papesch, head of the culture department in Gau Steiermark, to be replaced by the Nazi Wilfried Teppner. The museum was now answerable to Section II d of the Reichsstatthalter of Styria. Most of the acquisitions from Viennese collections seized and secured by the Nazis, such as those of Alphonse and Louis Rothschild, Oscar Bondy, Rudolf Gutmann and Albert Pollak, and also from Burgenland and Styrian estates, concerned the Joanneum's art and applied art collections. They played an important role in the development of the Neue Galerie founded in 1941. Acquisitions were made through a special "Judenkredit" (Jewish loan) item in the budget by Gau Steiermark granted annually to the museum for "the purchase of seized Jewish art objects". The academic personnel in the Joanneum were frequently called upon for their expert advice. For example, Karl Garzarolli-Thurnlackh, head of the Landesbildergalerie and from 1941 of the Alte Galerie, was a court-sworn general art expert at this time (paintings, sculptures and graphic art). As the Gau official responsible for art education and  Museumspfleger (special museum curator) for the district Styria, Hans Riehl, from 1941 head of the Neue Galerie, was involved in the acquisition of cultural items in Lower Styria. The first external depots for museum objects became necessary in autumn 1938, as the museum’s own depots were full on account of additions from the collections confiscated from St. Lambrecht and Admont abbeys. Preparations for storage in the event of air raids began in autumn 1939, with suitable sites being sought outside Graz and away from large towns and railway junctions. Until the end of the war, the Joanneum used over twenty-five storage sites throughout Styria. Art collections were stored in Stift Rein, Schloss Gutenberg by the Raabklamm, Forsthaus Gstatterboden, Propstei Aflenz, Pfarrhof Wildalpen, Propstei Zeiring, Schloss Pux near Teufenbach, Schloss Herberstein and Schloss Thal. The scientific collections were stored at Schloss Waldstein near Deutschfeistritz, Burg Rabenstein, Schloss Gutenberg an der Raabklamm and Schloss Hollenegg near Deutschlandsberg. Schloss Freibüchl/Gemeinde Hengsberg and Schloss Herberstein housed the archaeological and coin collections. Safes at banks in Graz were also used for these collections. According to a report in 1954, the Kulturhistorische Sammlung had seventeen external stores, including Stift Rein and Schloss Frauental an der Laßnitz. The Zeughaus collection was stored in Weissenegg, Stainz and Waasen castles, and the Volkskundemuseum inventory at Schloss Weyer near Frohnleiten. Only outsize, bulky and extremely fragile objects, such as the "Friedrichswagen" (c. 1450), which was walled in for protection, remained in Graz. After the war, all of the items had been returned by 1946.

After the war, a seven-member committee (Kuratorium) again headed the Joanneum. The department heads were responsible for recovering the stored objects, reorganizing the collections and dealing with the restitution of artworks and cultural objects expropriated during the Nazi era. By the end of the 1950s around 95 per cent of the objects from seized collections had been restituted. The Joanneum retained only donated objects and those that had not been reclaimed by their former owners. In 1971, the Styrian provincial government adopted new statutes for the Steiermärkisches Landesmuseum Joanneum, which included the appointment of a director. An unpaid committee (Kuratorium) appointed for five years would be available to provide assistance to the government.

At the beginning of April 1998, the Joanneum set up an in-house working group to investigate acquisitions and the restitution of Jewish property between 1938 and 1955. Initial research revealed that primarily three collections had acquired objects from expropriated collections: the Kulturhistorische Sammlung, Neue Galerie Graz and Alte Galerie. On the basis of the research report presented to the Styrian provincial government in 1999, on 14 March 2000 the Styrian parliament adopted the Provincial Constitutional Law on the Restitution of Suspicious Acquisitions from Property Expropriated during the Nazi Era. Since 2000, thirty objects have been returned to thirteen entitled heirs (in alphabetical order): the successors of Hugo and Margit Blitz, Oscar Bondy, Valerie Eisler, Leo Fürst, Rudolf Gutmann, Leo and Helene Hecht, Samuel Kiesel, Gottlieb and Mathilde Kraus, Aladar Latzer, Ernst Felix Pollack, Heinrich Rieger, Alphonse Rothschild and Leopold Weinstein. Provenance research in Joanneum continues on the basis of the Provincial Constitutional Law. In 2001 the Styrian provincial government decided to turn the Joanneum into a non-profit private limited company. This company was set up two years later with two managing directors. The province of Styria remains the owner of the real properties and has the rights to the museum's assets. In 2009 the museum was renamed Universalmuseum Joanneum.