The Senate Opposition Party Room was known as the Senate Club Room from the opening of Provisional Parliament House in 1927 to 1937. It was a place for Senators from all political parties to congregate in a relaxed atmosphere to converse, write letters, read, or to enjoy film nights. Use of the Senate Club Room was later restricted to opposition Senators, who had lost the use of their former party room after the 1929 election, since which time it has been known as the Senate Opposition Party Room.

The room featured comfortable club style lounges and easy chairs, tables, mail boxes, large glass-fronted bookcases and (a later addition) sound proof telephone boxes for Senators without their own office space. Private Members and Senators made use of their party rooms to attend to correspondence and any other business they needed to transact outside of Chambers while they were in Canberra: their principal workplace was the office accommodation provided for them in or near their electorates. Much of the original fabric and furniture has been retained in the Senate Opposition Party Room, making it one of the best preserved rooms in the building. According to Senator Doug McClelland, visiting the Senate Opposition Party Room in 2000, each Senator had two mail boxes, a small one for correspondence and a larger one for papers and the like, with the biggest mail boxes being allocated according to seniority. He believed that the room as at June 2000 was an accurate reflection of how it had looked during his time in opposition (intermittently from 1962-1987).

Immediately after the opening ceremony in the Senate in 1927, the Duke of York held a private ceremony in the Senate Club Room where he bestowed honours on 34 recipients who had been approved by King George V at New Year. Among those receiving honours were: Stanley Melbourne Bruce (Australia’s youngest Prime Minister, and in office for the opening of Provisional Parliament House), John Smith Murdoch (Architect of the building), Major John Henry Butters (Chief Commissioner, Federal Capital Commission), and Major-General Sir Cyril Brudenell Bingham White (Chief-of-Staff of the combined Australian Defence Forces).