In late 1940, the ILP-CCF accepted an offer by Manitoba Premier John Bracken to become part of an all-party "unity government".

This decision was opposed by some national leaders (including David Lewis), but was supported by local figures such as Seymour Farmer, who had led the ILP parliamentary group since 1935.

On November 4, 1940, Farmer became the first socialist politician in Canadian history to attain cabinet rank, having been sworn in as Minister of Labour.

For the next few years, the CCF's primary concern was preventing infiltration from Communists (then officially represented by the Labour Progressive Party).

This failure was due in part to the province's outdated electoral boundaries, which favoured rural ridings at the expense of the cities.

Stinson was probably the most adept of the Manitoba CCF's leaders, but he was unable to translate his personal popularity and charisma into victory at the polls.

The party fell to five seats in 1953, during the first election to be held after the province's Liberal-Conservative coalition dissolved amid acrimony.

Stinson was relatively popular among the province's "centre-left" voters, and the CCF increased its seat total to eleven in 1958.

The Campbell government initially attempted to stay in power through an alliance with the CCF, which turned down this offer (perhaps due to the disappointment of 1940–43).

The CCF was forced to lend support to Roblin's initiatives, thereby providing his ministry with the legislative record it needed to win a majority the following year.