Oliver was re-elected as a UFO MPP in 1929 and was the sole (and last) United Farmers member in the legislature until 1940. In that year, he formally joined the Ontario Liberal Party and the cabinet of PremierMitchell Hepburn as Minister of Public Works and Welfare after informally supporting the Liberals throughout the 1930s. Oliver quit the cabinet in late October 1942, in protest against Hepburn's leadership of the Liberal Party after Hepburn quit as Premier of Ontario but refused to resign as leader and appointed Gordon Daniel Conant as the new Premier without consulting the party. Oliver's resignation contributed to a crisis that eventually led to the both Hepburn and Conant's resignation and a leadership convention in May 1943 which was won by Harry Nixon. Oliver rejoined the cabinet under new Premier Harry Nixon as Deputy Premier but Nixon's government was short-lived going down to defeat in the October 1943 Ontario election.
Oliver became Liberal leader in 1945 and led the party through the 1948 Ontario election that again reduced the Liberals to third place behind the Tories and Ontario CCF. He resigned the leadership in 1950 and was replaced by Walter Thomson. However, Thomson was unable to win election to the Legislature, so Oliver remained house leader. He became party leader again from 1954 until 1957. Despite his experience, he was never able to lead his party to victory. Farquhar Oliver retired from the legislature in 1967, and died in 1989 at the age of 85.
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