[7][8] By 1977, she was working in Pittsburgh, Pennsylvania at KDKA-TV, spending 80-hour weeks hosting and producing their Evening Magazine show;[7] she and Stanley Hanover appeared to have separated.

[7] Hanover branched out into acting, having a prominent role as real-life presidential sister Ruth Carter Stapleton in the 1996 film The People vs. Larry Flynt;[10] noted critic Frank Rich called her performance brilliant.

[10][12] In April 2000, Hanover accepted the lead role in Eve Ensler's play The Vagina Monologues, a feminist work that was known for previously casting high-profile actresses such as Gillian Anderson, Melissa Etheridge, Calista Flockhart and Winona Ryder, among others.

[13] Veteran New Yorker contributor Peter J. Boyer asserted that Hanover's acceptance of the role was a "well-struck blow" because Ensler was "an outspoken critic of Giuliani's policies."

Before Hanover's debut, she postponed her participation in The Vagina Monologues on May 2 to support her husband a week after it was announced he had prostate cancer.

[14] On the evening after announcing his cancer diagnosis, reporters observed Rudy Giuliani having "a romantic dinner" with Judith Nathan, the woman who would be identified as his lover.

After ugly public battles between representatives of the two,[18] the divorce was finalized in July 2002 after he left office as Mayor; Hanover was awarded $6.8 million and custody of their two children.

[24] In May 2008 the two were replaced in the morning slot by the returning John R. Gambling, but she remained with the station as a film critic and fill-in host.

She was in the films Superstar with Will Ferrell in 1999, Keeping the Faith with Edward Norton in 2000, Someone Like You with Ellen Barkin in 2001, and Interview directed by Steve Buscemi in 2007.

Hanover played a Senator opposite John Goodman in an episode of Alpha House in 2014, and appeared in the TV comedy Odd Mom Out in 2015 and 2016.

[27] In 2011 she appeared in the off-Broadway initial run of "Picked", written by Chris Shinn and directed by Michael Wilson at The Vineyard Theatre.

Hanover made her Broadway debut in 2012 in Gore Vidal's The Best Man, directed by Michael Wilson and also starring James Earl Jones, Angela Lansbury, John Larroquette, and Candace Bergen.