Howarth was a Councillor on Cambridge City Council from 1987 to 2004, representing the city's Castle Ward. He was elected Leader of the Liberal Democrat group on Cambridge City Council in 1990 when it was in third place, and then leading it to become the principal opposition on the council, eventually becoming Leader of the Council in 2000. He continued as Leader until 2003, stepping down to concentrate on winning the Cambridge parliamentary seat. He stood unsuccessfully for Parliament in Cambridge in 1992 and 2001, and in the nearby seat of Peterborough in 1997. In the 2005 general election he was elected Member of Parliament for Cambridge, defeating Labour MP Anne Campbell, overturning a majority of 8,579, and winning with a majority of 4,339 votes (securing 44% of the votes cast). He was the first Liberal or Liberal Democrat to win Cambridge since the 1906 general election.