Having its origins as a castle chapel for the Berlin Palace, several structures have served to house the church since the 15th century.

The present collegiate church was built from 1894 to 1905 by order of Emperor William II according to plans by Julius Raschdorff in Renaissance and Baroque Revival styles.

In 1454 Frederick Irontooth, after having returned – via Rome – from his pilgrimage to Jerusalem, elevated the chapel to become a parish church, richly endowing it with relics and altars.

[3] Pope Nicholas V ordered Stephan Bodecker, then Prince-Bishop of Brandenburg, to consecrate the chapel to Erasmus of Formiae.

[4] On 7 April 1465 – at Frederick Irontooth's request – Pope Paul II attributed to St Erasmus Chapel a canon-law College named Stift zu Ehren Unserer Lieben Frauen, des heiligen Kreuzes, St. Petri und Pauli, St. Erasmi und St. Nicolai dedicated to Mary(am) of Nazareth, the Holy Cross, Simon Peter, Paul of Tarsus, Erasmus of Formiae, and Nicholas of Myra.

[5] On 20 January 1469, Dietrich IV, then Prince-Bishop of Brandenburg, invested eight clergymen, chosen by Frederick Irontooth, as collegiate canons with the prebends.

After his conversion he enriched the collegiate church with luxuriant furnishings, such as paraments, monstrances, relics, chasubles, carpets and antependia.

[9] In 1613, John Sigismund publicly confessed his Calvinist faith (in Germany usually called Reformed Church), but waived his privilege to demand the same of his subjects (Cuius regio, eius religio).

[9] In 1817, under the auspices of King Frederick William III of Prussia, the community of the Supreme Parish Church, like most Prussian Calvinist and Lutheran congregations joined the common umbrella organization named Evangelical Church in Prussia (under this name since 1821), with each congregation maintaining its former denomination or adopting the new united denomination.

In celebration of the Union Karl Friedrich Schinkel remodeled the interior in the same year and in 1820–1822 the exterior of Boumann's church in the neoclassicist style.

[9] The Supreme Parish and Cathedral Church faced at its southern façade Berlin City Palace, the residence of the Hohenzollerns (severely damaged in World War II and demolished later by the East German government), and the Lustgarten park at its western front, which is still there.

After dismantling the movable interior (altar, paintings, sarcophagi), Boumann's building was demolished in 1893 and Julius and Otto Raschdorff [de], father and son, built the present Supreme Parish and Cathedral Church in exuberant forms of high Neo-Renaissance style.

[13] The government of the Eastern German Democratic Republic did not oppose the work of the committee due to the concomitant inflow of Deutsche Marks.

Compared by some to the Medici Chapel, it had survived the war completely intact but was demolished for ideological reasons by the communist government due to it being a hall of honour for the Hohenzollern dynasty.

On 6 June 1993, the nave was re-inaugurated in an event attended by Federal Chancellor Helmut Kohl and televised nationwide in Germany.