Following Prime Ministerial Decree no. 171 of 29 August 2014, for the first time, non-autonomous Italian museums and places of culture were divided into 17 Regional Poli Museali (Museum Hubs). One of these is the Polo Museale del Lazio, responsible for over 46 museums and places of culture in Rome and Lazio that were previously assigned to 11 different superintendencies.

With the new ministerial reform introduced by Prime Ministerial Decree no. 169 of 2 December 2019, which entered into force on 5 February 2020, the establishment of the Regional Museum Directorates has led to creation of three new institutes from the previous Polo Museale del Lazio: the Lazio Regional Directorate of Museums, the State Museum Directorate of the city of Rome and the autonomous Vittoriano Museum and Palazzo Venezia.

With Ministerial Decree no. 22 of 28 January 2020, the Directorate of State Museums of the city of Rome has been recognised as a non-general executive level office.

The Direzione Musei statali della città di Roma has been operational since 31 March 2020 and its Director is Prof. Massimo Osanna.