Gyllenhaal expressed mixed feelings about the experience of being directed by Ang Lee in Brokeback Mountain but generally had more praise than criticism for Lee's directing style.While complaining of the way Lee tended to disconnect from his actors once filming began, Gyllenhaal praised his encouraging direction of the actors and sensitive approach to the material. I've never really been attracted to men sexually, but I don't think I would be afraid of it if it happened. The following year, Gyllenhaal played the lead role in the movie adaptation of the video game Prince of Persia: The Sands of Time, produced by Jerry Bruckheimer and released by Disney on May 28, 2010, and in the romantic comedy Love & Other Drugs, released on November 24, 2010, for which he received a Golden Globe Award nomination.Gyllenhaal received favorable critical reviews and an Evening Standard Theatre Award in the category "Outstanding Newcomer". He also auditioned to be Batman for the blockbuster Batman Begins and Heath Ledger play young men who meet as sheep herders and embark upon a sexual relationship that begins in the summer of 1963 and lasts for 20 years.

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He subsequently appeared in another indie film, The Good Girl (2002) and the climate fiction-disaster film The Day After Tomorrow (2004), portraying a student caught in a cataclysmic climate event.

In 2005, Gyllenhaal portrayed Anthony "Swoff" Swofford in Jarhead, Harold Dobbs in Proof, and Jack Twist in Ang Lee's Brokeback Mountain.

Rolling Stone critic Peter Travers praised Gyllenhaal's "exceptional" performance in the film.

Gyllenhaal joined John Mauceri and David Denby in Adam Gopnik's podium discussion in February 2016 at the David Rubenstein Atrium at Lincoln Center about Leonard Bernstein's breakthrough conducting performance in Carnegie Hall on November 14, 1943; accompanied by Jeanine Tesori on piano, he sang "Maria" from West Side Story.

For his performance in Brokeback Mountain, he received critical acclaim and won the BAFTA Award for Best Actor in a Supporting Role and was nominated for the Screen Actors Guild Award for Outstanding Performance by a Male Actor in a Supporting Role, the Satellite Award for Best Supporting Actor – Motion Picture, and the Academy Award for Best Supporting Actor.

Gyllenhaal received further recognition for roles in Zodiac (2007), Brothers (2009), Prince of Persia: The Sands of Time (2010), Love & Other Drugs (2010), for which he was nominated for the Golden Globe Award for Best Actor – Motion Picture Musical or Comedy, Source Code (2011), End of Watch (2012), Prisoners and Enemy (both 2013), Nightcrawler (2014), Southpaw (2015), and Nocturnal Animals (2016), for which he was nominated for the BAFTA Award for Best Actor in a Leading Role.

Gyllenhaal's performance was well received by critics; Gary Mairs of Culture Vulture wrote that "Gyllenhaal manages the difficult trick of seeming both blandly normal and profoundly disturbed, often within the same scene." After the critical success of Donnie Darko, Gyllenhaal's next role was as Pilot Kelston in 2002's Highway alongside Jared Leto.

His performance was described by one critic as "silly, cliched and straight to video".

Gyllenhaal later starred in the Touchstone Pictures romantic comedy Bubble Boy, which was loosely based on the story of David Vetter.

The film portrays the title character's adventures as he pursues the love of his life before she marries the wrong man.

The film earned million and was described in the Sacramento News and Review as Gyllenhaal's "breakout performance".