Watkins started his career with guest appearances on various television series including
Baywatch,
Get a Life,
Melrose Place, and
Sisters. He portrayed con-man
David Vickers on the
ABC soap opera
One Life to Live from 1994 to 1996, next joining the soap opera
General Hospital in the recurring role of Dr.
Pierce Dorman from 1996 to 1997. Watkins went on to star as Malcolm Laffley on the
Showtime series
Beggars and Choosers for its two-season run from 1999 to 2001. In 1999, he made his film debut in
I Think I Do, a small budget independent screwball romantic comedy, playing Sterling Scott, the soap opera hunk boyfriend of Bob, played by Alexis Arquette. He followed this with his first appearance in a big studio production,
The Mummy as the near-sighted glasses-wearing tomb raider Burns, later guest-starring on television series such as
NYPD Blue,
Six Feet Under, and
CSI: Crime Scene Investigation. After brief appearances in 2001 and 2002, Watkins rejoined the cast of
One Life to Live full-time from 2003 through 2006, with several short term returns to the show in 2007, 2008, and 2009, returning again on a regular basis beginning in June 2010.
Soap Opera Digest named Watkins's David their "Most Entertaining Male Character" of 2008, noting that "Time and time again, David's harebrained schemes and Tuc Watkins's side-splitting performances provide amusement we're always sorry to see end." On October 21, 2007, Watkins made his first appearance on ABC's Emmy-winning primetime series
Desperate Housewives as
Bob Hunter, a new resident of
Wisteria Lane who is a gay lawyer with a husband. He was a recurring character in seasons 4–6 and a series regular in seasons 7–8. On November 4, 2007, Watkins guest-starred on the
Cold Case season 5 episode "World's End". In July 2009, a
Funny or Die video called
The Sentimentalist starring Watkins was ranked number five on
Entertainment Weekly "The Must List", which notes the magazine's ten weekly choices among film, television, DVDs, books, music, and online entertainment for "The Top 10 Things We Love This Week". From 2007 to 2012, he continued his role of
Bob Hunter on
Desperate Housewives, staying with the show through its series finale on May 13, 2012. From 2012 to 2014, he played the recurring role of Pistol Pete on NBC's Emmy-nominated comedy series
Parks and Recreation. In 2012, he guest starred on several TV series, including
Franklin & Bash as Lance, ''
as Dr. Brett Denning, and Baby Daddy'' as Hank. In 2013, he guest starred on
Maron as Jerry,
Warehouse 13 as Nate, and
Anger Management as Jeff. In 2014, he played the recurring role of Joe Miller on the MTV series
Awkward. In 2015, he played the recurring role of Judge Stephen Schaeffer on the TNT series
Major Crimes. In 2016, he guest starred on ''
It's Always Sunny in Philadelphia as Scott and on Ballers'' as Jim. In 2017, he guest starred on
EastSiders as Patrick. In 2018, he played Hank in the 2018
Broadway revival of
The Boys in the Band. It was directed by
Joe Mantello and opened in previews at the
Booth Theatre on April 30, 2018, officially on May 31, and ran until August 11, 2018. This production, staged for the 50th anniversary of the play's original premiere, starred
Matt Bomer,
Jim Parsons,
Zachary Quinto,
Andrew Rannells,
Charlie Carver,
Robin de Jesús,
Brian Hutchison,
Michael Benjamin Washington, and Watkins. All of the actors who were in the 2018 production are openly gay. This production won the 2019
Tony Award for Best Revival of a Play. In 2020, Watkins reprised his role as Hank in the
Netflix film
The Boys in the Band. The film stars the full roster of players from the play's 2018
Broadway revival, comprising a cast of exclusively openly-gay actors, including
Jim Parsons,
Zachary Quinto,
Matt Bomer,
Andrew Rannells,
Charlie Carver,
Robin de Jesús,
Brian Hutchison,
Michael Benjamin Washington, and Watkins. The film was released on September 30, 2020, on
Netflix and received positive reviews from critics. Also in 2020, he began portraying Congressman Roger Harris on season 2 of
Showtime's Emmy-nominated comedy series
Black Monday. The series stars
Don Cheadle,
Andrew Rannells,
Regina Hall,
Casey Wilson, and
Paul Scheer, and follows the employees of second-tier Wall Street trading firm the Jammer Group during the year leading up to "
Black Monday", the day when international stock markets crashed in 1987. In 2021, he began portraying Troy on the hit HBO MAX comedy series
The Other Two, starring
Heléne Yorke,
Drew Tarver,
Ken Marino, and
Molly Shannon. In 2022, he began portraying Colin McKenna on the Netflix comedy series
Uncoupled, created by
Darren Star and
Jeffrey Richman. Watkins plays
Neil Patrick Harris's ex-boyfriend of 17 years. The series premiered on
Netflix on July 29, 2022, to critical acclaim. ==Personal life==