Following Davis's resignation as PC leader and as premier, Timbrell sought the party leadership at the January 1985 leadership convention. He positioned himself as a centre-right candidate - further to the right of Red Tory rivals Larry Grossman and Roy McMurtry, but not as far to the right as Frank Miller - and therefore the candidate best able to continue Davis' pragmatic, successful style of government.. Timbrell was the only candidate to favour eliminating rent controls during the campaign. His supporters included Keith Norton, Leo Bernier, Margaret Birch, Robert Eaton, Gordon Dean, Bob Welch and Norm Sterling. Timbrell placed second on the first ballot, but was eliminated when he fell to third place on the second ballot, six votes behind Grossman who had the backing of McMurtry's campaign. Dr. John Balkwill in 1987 claimed that 30 to 40 Miller supporters were instructed by the Miller campaign to vote for Grossman on the second ballot to prevent him from advancing. Lou Parsons, a senior Miller adviser, later acknowledged, "We wouldn't have won it against Dennis Our winning strategy was always to be against Larry... and in the end we were lucky." Timbrell reluctantly endorsed Grossman after the results were confirmed by a recount. He however did not bring enough delegates on the third ballot and that resulted in Miller's victory. He was retained in Miller's cabinet as Minister of Municipal Affairs and Housing with responsibility for Women's Issues.
Second leadership campaign
The Progressive Conservative Party under Miller's leadership was reduced to a narrow minority government in the 1985 election. Following a cabinet shuffle on May 17, 1985, Timbrell retained his previous postings and was additionally appointed Provincial Secretary for Resource Development. Miller's government was defeated in the House in June, 1985. In opposition, Timbrell served as House Leader of the Official Opposition and his party's critic for Education and Women's Issues. Miller resigned as leader, and the party called another leadership convention for November 1985. This contest was an extremely divisive struggle between Timbrell and Grossman, which exposed deep divisions in the party. A third candidate, Alan Pope, drew attention to the animosity between the candidates with his slogan, "Don't choose sides, choose Pope". Alan Eagleson was a co-chairman of Timbrell's campaign. In this leadership race, Timbrell announced he would not support the full funding of Catholic schools unless amendments were put forward guaranteeing entry to non-Catholic teachers and students. Norm Sterling, an inveterate opponent of Catholic school funding, derided Timbrell's position as opportunistic and crossed over to Grossman. Timbrell's change of position may have turned away other potential supporters as well. Pope finished third on the opening ballot and some believed that he could have given Timbrell a second-ballot victory over Grossman, though Pope chose not to endorse either side. Grossman defeated Timbrell on the second ballot by nineteen votes, effectively ending Timbrell's career in provincial politics. He did not seek re-election in 1987.
Timbrell served as president of the Ontario Hospital Association from 1991 to 1995. He also served as a Director of the St. Joseph's Health System from 1986 to 1988 and a Director of the Toronto School of Theology from 1986 to 1992 and in 1997–2003. He has served as a Director of various corporations, including Cabot Trust, Confederation Leasing, Confederation Trust, Ontario Blue Cross, United Telemanagement Corporation and Eco Power Solutions Inc.
In 2006, Toronto City Council voted to name the community recreation - library - aquatic - child care facility, located at 29 St. Dennis Drive, Don Mills the "Dennis R. Timbrell Resource Centre in Flemingdon Park". Timbrell has received the following forms of recognition: 1977 - The Queen's Silver Jubilee Medal 1978 - Officer of The Order of St. John of Jerusalem 1992 - The Canada Confederation 125 Medal 1993 - Knight of Malta 2012 - The Queen's Diamond Jubilee Medal
