Churchill was a key adviser to Progressive Conservative Party leader John Diefenbaker during this period, and was widely credited with developing the strategy that propelled the Tories to victory in 1957.

Prior to the 1957 election, Churchill wrote a confidential paper arguing that the Progressive Conservative Party could form government by targeting seats in the English-speaking provinces, and did not need to invest resources in Quebec.

The Progressive Conservatives were re-elected with a large majority in the 1958 federal election; Churchill defeated his nearest opponent in Winnipeg South Centre by almost 20,000 votes.

Churchill gave approval in 1959 for Canada's first commercial power nuclear reactor, a CANDU design, to be built at Douglas Point, Ontario.

[2] The Progressive Conservatives were reduced to a minority government in the 1962 federal election; Churchill's majority in Winnipeg South Center shrank to 2,000 votes.

He had served only two months in this position when the Progressive Conservatives were defeated in the 1963 federal election; Churchill was personally re-elected with an even smaller majority.

The Ottawa Citizen quoted him describing Prime Minister Lester Pearson as "a sawdust Caesar, reminding me of Mussolini, trying to force the country to accept his personal choice for a flag.

[6] In February 1968, Churchill attacked new Progressive Conservative leader Robert Stanfield for not forcing an election when the Liberal government of Lester Pearson was unexpectedly defeated in the house.