Jenkins slowly began building more TV and feature credits in the early 1980s, including turns as Veronica Cartwright's husband in "The Witches of Eastwick" (1987) and a string of cops, agents, and other serious types in "Little Nikita" (1988), "Sea of Love" (1989), and the TV-movie "Challenger" (1990), in which he played engineer Gregory Jarvis, who perished aboard the space shuttle when it exploded in 1986. After a decade of mostly dramatic roles, Jenkins earned his widest notices for David O. Russell's "Flirting With Disaster," a smart comedy of errors with an all-star cast, including Ben Stiller, Patricia Arquette, Lily Tomlin, Alan Alda, and George Segal. However, Jenkins received some of the best reviews for the film as a by-the-books DEA agent who not only revealed that he was in love with his partner (Josh Brolin), but experienced a show stopping acid freakout in the film's final third. The dichotomy between Jenkins' staid exterior and his unbridled performance yielded considerable laughs - as well as a 1997 Independent Spirit nomination - and roles in comedies soon began popping up between his more straight-laced performances. He was well utilized by Bobby and Peter Farrelly, who first cast him in an uncredited turn as a psychiatrist in "There's Something About Mary" (1999) before tapping him for supporting turns in their Jim Carrey feature "Me, Myself and Irene" (2000) and as the stroke-stricken dad to Heather Graham in "Say It Isn't So" (2001).

Another set of famous filmmaking siblings - Joel and Ethan Coen - also made excellent use of Jenkins' versatile skills. The filmmakers first became aware of him after he auditioned for William H. Macy's role in "Fargo" (1996), but did not cast him in one of their films until their neo-noir "The Man Who Wasn't There" (2001), where he played the hard-drinking lawyer father to femme fatale Scarlett Johansson. Two years later, he turned up as a more sober legal figure in "Intolerable Cruelty" (2003), the Coen's lightweight tribute to screwball comedies, and reunited with them in 2008 as a gym manager in the dark comedy "Burn This," about a former CIA agent (John Malkovich) who loses his memoirs to a pair of Jenkins' employees (Brad Pitt and Frances McDormand).

In 2001, Jenkins began the first of several recurring appearances on the acclaimed HBO series "Six Feet Under." His character, Nathaniel Fisher Sr., was killed in a horrific traffic accident within the first 10 minutes of the pilot episode, but returned sporadically throughout the series' run to impart advice and warnings to his eldest son Nate (Peter Krause) from beyond the grave. His appearances underscored the series' theme of regret and loss, as the conversations (imagined or not) revealed that the elder Fisher had a rich and occasionally wild hidden life that belied the bland, emotionless exterior he showed to his family. Jenkins was nominated along with the rest of his "Six Feet Under" castmates for a 2002 Screen Actors Guild award.

The acclaim of these and other projects helped to make Jenkins one of the busiest character actors in Hollywood, and one of the most well-regarded. He received some of his best notices for "North Country" (2005) as a father who slowly rises to the defense of his daughter (Charlize Theron) when she is assaulted at her mine working job. In 2007, actor Tom McCarthy cast Jenkins in his first leading role for "The Visitor," an affecting drama about a mild-mannered professor whose empty life is suddenly enriched by the presence of three Syrian immigrants facing deportation. Jenkins suddenly found himself the subject of numerous interviews and on the receiving end of considerable praise, include the top prize from the Method Fest in 2008. He also earned nominations for both the Independent Spirit and Screen Actors Guild awards. But most importantly, he received his first ever Academy Award nomination.

True to form, Jenkins balanced this soulful performance with a pair of comedies - as the stepfather to Will Ferrell in the Farrelly Brothers' comedy "Step Brothers" (2008), and the aforementioned "Burn This." Ferrell and "Step Brothers" director Adam McKay were reportedly so taken with Jenkins' performance that they featured him in several short comic films on their web site, funnyordie.com. One such short, "Hollywood Tales with Richard Jenkins," had the actor spinning outrageous stories of missed opportunities, including a chance to "make it with Michelle Pfeiffer in "The Witches of Eastwick."