Acting
Without an agent, Lindhome started her acting career with a role in a short film Backseat Detour (as a backseat passenger), and as Charlie in the sitcom Titus. In a season seven episode of the TV series Buffy the Vampire Slayer she was the crutches-using student Cheryl in 2002. In 2003, she joined The Actors' Gang and appeared in the play Embedded in two roles (a commedia dell'arte of Condoleezza Rice, and a reporter) and was one of four actors from the play to be cast in the 2004 Academy Award-winning film Million Dollar Baby, where she played Mardell Fitzgerald, the trailer-living sister of Maggie, the film's lead.
Lindhome briefly appeared as a nameless inquisitive student in a season three episode of the television series Gilmore Girls in 2002 before later guest-starring as calorie-counter Juliet on the show's fifth and sixth seasons. She also appeared as Janelle in the 2006 techno-horror film Pulse and as a cruel nurse in the 2008 crime drama film Changeling. She guest-starred on the television series The Big Bang Theory as Ramona Nowitzki, a controlling graduate student obsessed with Sheldon Cooper, in seasons two, ten and eleven (2008, 2017). She guest-starred in the television series Pushing Daisies as the pie-loving Jeanine. In 2008, she played Hilary, a devout Christian girl who has a purposely disastrous date with Dane Cook in My Best Friend's Girl; and had a minor role as murder victim Vanessa Holden on the crime drama series Criminal Minds. In 2009, she starred as the vicious, amoral Sadie in The Last House on the Left, a remake of the 1972 horror film of the same name.
In 2011, Lindhome was featured alongside Heather Morris, Sofía Vergara and Ashley Lendzion in "Nuthin' But a Glee Thang", a Glee-themed Funny or Die parody of the Dr. Dre song "Nuthin' but a 'G' Thang". From 2010 to 2013, she developed and hosted the Nerdist podcast Making It with Riki Lindhome, interviewing people in the entertainment industry about their rise to fame. From 2011 to 2013, she guest-starred as Harper on the HBO television series Enlightened. She played a female version of Conrade, one of Don John's followers with whom he has a steamy relationship in Joss Whedon's Much Ado About Nothing, and appeared as the "Galaxy Scout" costume-wearing Denise in the 2012 comedy film Fun Size. In 2013, she starred in the horror-comedy film Hell Baby as Marjorie, the protagonist's Wiccan sister, a role for which she did a full frontal nude scene that attracted attention for being unusually lengthy.
In 2015, Lindhome and Natasha Leggero created the Comedy Central series Another Period, in which Lindhome also starred as Beatrice Bellacourt. The show, which focuses on the Bellacourts, a fictional aristocratic family living in Newport, Rhode Island at the turn of the 20th century, premiered in June 2015. She had a recurring role on the television series The Muppets in 2015 as Becky, Fozzie Bear's human girlfriend. Also in 2015, she appeared in a season two episode of Fresh Off the Boat as Arielle, a resort masseuse, and Agneta, a Swedish Detective in Brooklyn Nine-Nine's season three episode "The Swedes". She voiced Poison Ivy in the 2017 animated film The Lego Batman Movie.
In 2018, Lindhome guest-starred as Shaina, a recovering drug addict, in an episode of the comedy-drama television series Kidding., and later in 2018, Lindhome played "The Actress" who has casual sex with the "aimless" Sam in the neo-noir black comedy Under the Silver Lake. In October 2019, she was featured in SoulPancake's short documentary film Laughing Matters. The next month, she appeared in the ensemble cast of the 2019 mystery film Knives Out as faithful wife Donna Thrombey. She began starring in the Fox animated sitcom series Duncanville in February 2020, voicing the character Kimberly Harris, the emotional 12-year-old sister of the protagonist, Duncan Harris. In October 2020, she starred in the comedy thriller film The Wolf of Snow Hollow, directed by Jim Cummings, as sympathetic yet professional local police officer Julia Robson.
In 2022, she voiced Royal Assistant Beep Beep in the Warner Brothers animated comedy film King Tweety, and starred as Dr. Valerie Kinbott, Wednesday Addams's strict but understanding court-ordered therapist, in the Netflix comedy horror series Wednesday.
In 2023, she guest-starred as Justine the Belieber, a fan of Justin Bieber who steals Dr. Teeth's van in Disney's The Muppets Mayhem.
In 2024, she appeared as Maud in the horror film Afraid.
