Colfer’s first TV role came in 2009 when he was cast as Kurt Hummel on Fox’s Glee. Kurt is a fashionable gay countertenor who is routinely bullied at school for being gay and participating in the very unpopular Glee Club. Colfer auditioned for the part of Artie Abrams, who uses a wheelchair, a role which eventually went to Kevin McHale.

In an interview with Chelsea Handler in December 2009, Colfer stated that he is gay. He has been in a relationship with actor and producer Will Sherrod since 2013.

In a 2010 interview with Allison Kugel, Colfer stated that:

Colfer appeared on the British chat show Friday Night with Jonathan Ross in June 2010, together with his fellow Glee co-stars Amber Riley and Matthew Morrison. He demonstrated his skill with a pair of sai, revealing that he bought a pair on eBay and regularly practices in his trailer. He also mentioned that he would like it if his sai could be worked into an episode of Glee; they first appeared in the season 3 episode “I Am Unicorn”, during Colfer’s character Kurt Hummel’s performance of “I’m the Greatest Star” from the musical Funny Girl.

On June 8, 2011, Colfer signed a book deal with Little, Brown and Company to write two novels for children. The first book in the series, The Land of Stories: The Wishing Spell, was released on July 17, 2012. The books are about two twins, named Conner and Alex Bailey, who get their grandma’s book and go through adventures in “The Land of Stories”. For two weeks after the book’s release it was number one on The New York Times Best Seller list in the Children’s Chapter Books category.

At an early age, Colfer showed a passion for writing. He was “born wanting to be a storyteller”, using both writing and acting as ways to entertain people and escape reality. His grandmother was his first editor, advising and encouraging him in elementary school when he first attempted to write a fairytale-inspired novel, which would later become The Land of Stories. In 2012, Colfer dedicated his first published novel to her, and quoted her: “Christopher, I think you should wait until you’re done with elementary school before worrying about being a failed writer.”

Colfer wrote, starred in, executive-produced, and novelized the coming-of-age comedy film Struck by Lightning. The plot revolves around Colfer’s character, who is struck and killed by a bolt of lightning, and chronicles his exploits as he blackmails his fellow senior classmates into contributing to a literary magazine he is publishing. It was shot during the Glee hiatus in the summer of 2011 and had its world premiere in 2012 at the Tribeca Film Festival.

In March 2012, Colfer was featured in a performance of Dustin Lance Black’s play, 8 – a staged reenactment of the federal trial that overturned California’s Prop 8 ban on same-sex marriage – as Ryan Kendall. The production was held at the Wilshire Ebell Theatre and broadcast on YouTube to raise money for the American Foundation for Equal Rights.

In 2012, Colfer released a companion book to his film Struck by Lightning, called Struck By Lightning: The Carson Phillips Journal.

In 2013 and 2014, Colfer won consecutive People’s Choice Awards for Favorite Comedic TV Actor. Both speeches he gave were praised by the media for being funny while making references to things like fanfiction and fanart to show his appreciation for fan culture.

In 2013, Colfer filmed a public service announcement (PSA) with Elmo about anti-bullying for Sesame Street in Communities, and participated in the Course of the Force run benefiting the Make-A-Wish Foundation. In 2014, he participated in a PSA about Let Girls Learn, put out by the U.S. Agency for International Development. On Hollywood Game Night, hosted by Glee co-star Jane Lynch, Colfer won $6,000 and donated it to the Make-a-Wish Foundation of America.

Colfer was a co-chair for the Elton John AIDS Foundation Academy Award Party in 2013 and 2014. He is a coalition member of Uprising of Love, an organization which supports the safety and dignity of Lesbian, Gay, Bisexual, Transgender, and Intersex (LGBTI) Russians.

The third book in the series, The Land of Stories: A Grimm Warning, was released on July 8, 2014. Now considered a series, it reached No. 4 on The New York Times Best Seller list and spent four weeks on the list.

On January 28, 2014, it was announced that Colfer will star in a new 3D CG animated family film by Marza Animation Planet, Robodog, as the voice of the title character. The film, which will costar Ron Perlman, is described as “a classic, heart-warming adventure story about an unlikely duo who couldn’t be more different.” The film’s director, Henry F. Anderson III, said Colfer is “perfect” for the project because he “has an appealing, youthful voice which fits right in with our lead character, KC, who is above all a charismatic entertainer.” Vocal recording for the film began on February 1, 2014. The film is now in post-production, though as of 2019 no release date has been set.

After a few months of planning, it was revealed in March 2014, that Colfer had been asked by Glee’s producers to write an episode. About the offer, Colfer said: “I’ve been asked in interviews if I ever wanted to write [an episode of Glee], and I said, ‘Absolutely not because it was not my world.’ I didn’t want to tamper with someone else’s image. Then they were like, ‘Here, come tamper.'” The title of the episode, which aired in May 2014, is “Old Dog New Tricks”.

In 2014, Colfer guest starred on an episode of Hot in Cleveland as Tony, Victoria’s son. In March 2015, Jane Leeves posted an image on Twitter confirming that Colfer would be returning to an episode titled “All About Elka” in the show’s final season.

Colfer’s fourth novel, The Land of Stories: Beyond the Kingdoms, was released on July 7, 2015. Following its release, The Land of Stories charted at No. 1 as a series on The New York Times Best Seller list for the first time on July 26.

The picture book, written by Colfer and illustrated by Brandon Dorman, The Curvy Tree was released in October 2015, and is based on a short original fairy tale of the same name, which Colfer first told in The Land of Stories: The Wishing Spell.

On May 14, 2015, it was made public that the biopic Colfer has been mentioning for almost a year was going to be about Noël Coward with the working title Noel with Colfer in the title role. Colfer prepared for the role in London. The film will be directed by Joe Stephenson. While filming was expected to begin sometime during the summer of 2015, it has been delayed.

The fifth book in the series, The Land of Stories: An Author’s Odyssey, was released on July 12, 2016. The sixth and final installment, The Land of Stories: Worlds Collide was released on July 11, 2017.

In 2016, he played Christopher in Absolutely Fabulous: The Movie. He had been offered the role by Jennifer Saunders after he invited her to the Glee: Live tour in 2011. He also appeared as a guest judge in Chopped Junior.

In June 2017, it was announced that Colfer will make his directorial debut with a film adaptation of The Land of Stories: The Wishing Spell. He will also write the script and serve as one of the executive producers on the project.

In 2017, Colfer announced he is developing a new TV show called Indigo, a sci-fi drama about indigo children who are misdiagnosed as having mental or physical illnesses – when they really possess supernatural abilities. “In addition to starring in the project – which will be shopped around to broadcast networks, cable channels and streaming services – Colfer is also expected to write and direct the pilot, which he’ll executive-produce alongside Keith Quinn and Rob Weisbach.”.

In early 2017, Colfer released his second book for young adult readers called Stranger Than Fanfiction. This book follows the story of Cash Carter, a world-famous television star who decides to take a cross-country road trip with four of his biggest fans, as they are getting ready to enter college.

On October 1, 2019, Colfer came out with a new book, A Tale of Magic. It is a prequel to the Land of Stories series.