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In October 2017, Benoist helped with Chris Wood's launch of his website "I Don't Mind" that works to put a stop to the stigma around mental illnesses, admitting that she has struggled with depression and anxiety attacks since she was 13 years old. She said that Wood's words enabled her to admit her own issues with depression to others. Benoist and Wood announced their engagement on February 10, 2019, and married in September 2019. On March 4, 2020, the couple announced on Instagram that they were expecting their first child.

On stage, Benoist made her Broadway debut in 2018 as Carole King in the jukebox musical Beautiful: The Carole King Musical.

On May 7, 2018, it was announced that Benoist would be playing the titular character in the Broadway show Beautiful: The Carole King Musical at the Stephen Sondheim Theatre, which marked her Broadway debut for a limited run from June 7 through August 4, 2018.

In April 2017, Benoist was cast as Rachel Koresh, the legal wife of Branch Davidian cult leader David Koresh in Paramount Network's miniseries Waco. Benoist was featured in "The Super Duper Minecraft Musical!" which was made for Minecraft's Super Duper Graphics Pack in November.

In May 2016, Benoist was cast as Katherine Russell, the widow of deceased Boston Marathon bomber Tamerlan Tsarnaev, in Peter Berg's drama film Patriots Day. In June, it was announced that she was set to star in the comedy-drama film Sun Dogs. Also in that month, the Human Rights Campaign released a video in tribute to the victims of the 2016 Orlando gay nightclub shooting; in the video, Benoist and others told the stories of the people killed there.

She had a role in the 2015 film Danny Collins. She played the part of Jamie, a desk clerk at a hotel frequented by one of Jamie's all-time favorite rock stars. That same year, Benoist also played Becky Thatcher in Band of Robbers, a modern-day retelling of The Adventures of Tom Sawyer and Adventures of Huckleberry Finn. In May 2015, it was announced that Benoist would be playing Lorelai in the film Low Riders, replacing Lily Collins and Nicola Peltz, who were in talks for the role previously. In August of that year, she landed the leading role in the Screen Gems drama feature film Oxford.

In October 2015, the superhero adventure series Supergirl, with Benoist in the lead role of Kara Zor-El, premiered on CBS. She became the first woman to lead a prime time superhero TV series since Wonder Woman went off the air in 1979. The premiere was watched by 12.96  million viewers and received a full season order by CBS on November 30, 2015. She was reportedly the first actress looked at for the role. Benoist generally received positive reviews for her portrayal of Kara Zor-El. The series later moved to The CW before its second-season premiere. She reprised her role in The CW's Arrowverse crossovers "Invasion!", "Crisis on Earth-X", "Elseworlds", and "Crisis on Infinite Earths" as well as The Flash episode "Duet". She reprises her role as Earth-X's Supergirl doppelgänger Overgirl in the CW Seed animated series Freedom Fighters: The Ray. The actress will make her directorial debut for one episode during season five.

In 2015, it was announced that she and her Glee co-star Blake Jenner were married. Benoist commented that they had been married "longer than anybody knows", with some sources claiming that the couple actually wed the same year of their engagement in 2013. In late December 2016, she filed for divorce citing "irreconcilable differences". The divorce was finalized in December 2017.

Also in 2015, Benoist suffered an injury that tore her iris. The incident caused one pupil to be permanently enlarged. In November 2019 in an Instagram video, Benoist revealed that the injury to her iris was due to an iPhone being thrown at her during a domestic dispute, in a relationship marked by repeated domestic violence. Previously, the injury had been said to have been caused when she tripped down stairs and fell into a potted plant.

Benoist rose to prominence for her portrayal of Marley Rose on the Fox musical comedy-drama television series Glee (2013–2014). She appeared in films such as Whiplash (2014), Danny Collins (2015), The Longest Ride (2015), Patriots Day (2016), Lowriders (2016), and Sun Dogs (2017), and she portrayed David Koresh's wife Rachel Jones in the miniseries Waco (2018).

In mid-2013, Benoist and Blake Jenner held a Kickstarter campaign to help fund the production of their feature film Billy Boy. The project reached its $100,000 goal. Benoist played Nicole in the 2014 independent drama film Whiplash, which won top prizes (Grand Jury and Audience awards) at the 2014 Sundance Film Festival. In June 2014, she joined Nicholas Sparks' film adaption The Longest Ride as Marcia.

In May 2012, she auditioned for the musical comedy-drama series Glee in New York at the Roundabout Theatre Company, singing a different song for each of her five auditions including: "Fidelity" by Regina Spektor, "King of Anything" by Sara Bareilles, a Colbie Caillat song, and several musical theatre pieces. In July, she had two screen tests in California for series creator/writer, Ryan Murphy, the casting directors, and executive producers. She portrayed Marley Rose on the fourth and fifth seasons of Glee. Her first appearance as Marley Rose was in the first episode of season four, titled "The New Rachel". Because the creators had been looking for Marley for a long time, she started working the day she found out she got the job. Benoist's first performance was a duet of "New York State of Mind" with Lea Michele, during the first episode of season 4. The cover of the song reached twenty-four on the Bubbling Under Hot 100 Singles chart. She and Glee co-star Darren Criss appeared with Josh Duhamel in the opening of the 2013 Kids' Choice Awards. That same year, she was selected as an ambassador for Coca-Cola's new product, P10 300 mL Coke Mismo. In June 2013, they were flown to Manila, Philippines, to endorse the product by visiting various malls and meeting with fans. She left the series Glee in early 2014, along with several other actors.

Benoist's first film was in Tennessee in 2008 along with singer Mariah Carey. Afterwards, she made guest appearances on shows like Law & Order: Criminal Intent, Blue Bloods and The Good Wife, while attending college. She played Kelly in the 2011 Goodspeed Musicals theatrical production of The Unauthorized Autobiography of Samantha Brown by Brian Lowdermilk and Kait Kerrigan at the Norma Terris Theatre.

In 2006, The Denver Post named Benoist one of Colorado's five "Can't Miss Kids". She graduated from Arapahoe High School in Centennial, Colorado, in 2007, and then she moved to New York City to pursue a career in musical theatre. She initially attended Marymount Manhattan College for the BFA musical theatre program but in her sophomore year, she switched majors to straight theatre, due to her admiration for 19th-century Russian plays. She graduated from Marymount Manhattan College with a Bachelor of Arts in Theatre Arts in 2011. While attending Marymount Manhattan college, she played the titular characters Millie Dilmount in an urban off-off-Broadway production of Thoroughly Modern Millie and Rosalind in As You Like It at the Theresa Lang Theatre.

Melissa Marie Benoist (/b ə ˈ n ɔɪ s t / ; born October 4, 1988) is an American actress and singer. She has performed on stage and in television and film. She is known for her portrayal of the titular character in the CBS/CW DC Comics–based superhero drama series Supergirl (2015–present).