Two years later, he became a more senior whip with the title Junior Lord of the Treasury until the Conservatives' defeat, in the 1929 general election.
Following the November 1931 general election, he was promoted to the senior position of Parliamentary Secretary to the Treasury (Government Chief Whip).
That proved tricky several times, as different sections of the National combination came to denounce areas of government policy.
Margesson adopted a method of strong disciplinarianism combined with selective use of patronage and the social effect of ostracism to secure every vote possible.
However, a major faultline lay over the question of introducing protective tariffs on imports as a prelude to negotiating a customs union within the British Empire.
Whilst the Liberals themselves barely commanded the support of 33 MPs, they were one of only two parties in the government with a long independent history, and there were fears that their withdrawal would turn the National Government into a mere Conservative rump, something that National Labour Prime Minister Ramsay MacDonald wished to avoid.
Many believed that the plan would not have been pursued except for both a desire to prove the government's nonpartisan credentials and Conservative leader Stanley Baldwin's determination to implement the policy.
Opponents to Indian Home Rule found several spokespersons, most notably Winston Churchill, and they harried the government at every stage, with nearly one hundred Conservative MPs voting against the third reading of the Bill, the highest number of Conservatives to vote against a three-line whip in the twentieth century.
Margesson was retained as Chief Whip when Baldwin became Prime Minister in June 1935 but had to face further rifts in the party over foreign policy and other matters.
In December, the leaking of the proposed Hoare-Laval Plan to grant two-thirds of Abyssinia to Italy outraged some Conservative MPs.
However, a well of discontent with the government's foreign policy grew, especially after Britain entered World War II.
Margesson was referred to in the book "Guilty Men" by Michael Foot, Frank Owen and Peter Howard (writing under the pseudonym "Cato"), published in 1940 as an attack on public figures for their failure to re-arm and their appeasement of Nazi Germany.
Margesson, who was living at the Carlton Club since his recent divorce, was present when it was bombed by the Luftwaffe on 14 October 1940.
Margesson proved competent and efficient, but in February 1942, Britain suffered severe military setbacks, including the loss of Singapore.
Lord Margesson died in the Bahamas in December 1965, aged 75, and was succeeded in the viscountcy by his only son, Francis.