Toxopeus became as a Member of the House of Representatives shortly after the election of 1956 when the number of seats was increased from 100 to 150 on 6 November 1956 and served as a frontbencher and spokesperson for Law Enforcement and Spatial Planning.

On 1 October 1969 Toxopeus unexpectedly announced he was stepping down as Leader but continued to serve in the House of Representatives as a backbencher until his resignation on 1 November 1969.

Toxopeus continued to be active in politics and in January 1970 was nominated as the next Queen's Commissioner of Groningen serving from 16 February 1970 until 1 November 1980.

Toxopeus also became active in the private and public sectors as a corporate and non-profit director and served on several state commissions and councils on behalf of the government.

Toxopeus granted the honorary title of Minister of State on 22 January 1985 and continued to comment on political affairs as a statesman until his death in August 2009 at the age of 91.

He holds the distinction as the longest-serving Minister of the Interior after World War II with 5 years, 330 days.