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Cotterill joined the [[New Zealand Labour Party|Labour Party]] in 1928 and became secretary of first the Wanganui East branch and later the Wanganui LRC. At the 1933 local-body elections he was elected to both the Wanganui City Council and Power Board, sitting on the bodies until 1938. In 1944 he was elected to the Wanganui Harbour Board, serving a three year term.{{sfn|Gustafson|1986|pp=279}} He served in the [[New Zealand Army]] during [[World War II]] and was also the first chairman of the Wanganui rehabilitation committee when it was established in 1943, serving as its head for many years.<ref name="Obit"/>
He represented the [[Whanganui (New Zealand electorate)|Wanganui]] electorate from [[1935 New Zealand general election|1935]] to 1960, when he retired for family reasons, by which time he was Wanganui's longest ever serving MP.{{sfn|Wilson|1985|pp=190}} He became Labour's junior whip in 1951 and was senior whip from 1952 until 1958.{{sfn|Wilson|1985|pp=279}} Cotterill was regarded as one of the best
Cotterill was particularly interested in foreign affairs and spoke frequently on the topic in parliament. During the Second Labour Government he was chairman of Parliament's External Affairs Committee. In 1960 he represented the government at the opening of the third [[Cook Islands]] Legislative Assembly. He was also New Zealand's representative at two [[Commonwealth of Nations|Commonwealth]] association conferences, in [[Ottawa]] in 1952 and [[Kampala]] in 1960.<ref name="Obit"/>
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