Additionally, Howard directed the documentary film Dads (2019), and episodes of the Disney+ space western series The Mandalorian (2019–present) and The Book of Boba Fett (2022).

[6] Howard and her siblings were raised away from the world of show business; their parents did not allow them access to television, and instead encouraged outdoor activities and hobbies.

[7] Howard began training as an actor at Stagedoor Manor, a performing arts camp in upstate New York, alongside Natalie Portman.

In 2003, Howard performed as Rosalind in the William Shakespeare comedy As You Like It at The Public Theater, where she caught the attention of film director M. Night Shyamalan, who two weeks later and without an audition, cast her in his fantasy thriller The Village (2004).

[21][22] Howard again portrayed Rosalind in Kenneth Branagh's 2006 film adaptation of Shakespeare's As You Like It, which was released theatrically in Europe before premiering on HBO in the United States.

[26] That year, she wrote and directed a short film called Orchids as part of Glamour magazine's "Reel Moments" series, which was funded by Cartier and FilmAid International.

[28] Howard described herself as a "huge fan" of the franchise and did extensive research to prepare for the role, including reading comic books and dyeing her hair blonde for the part.

[32][33] Howard then starred in the science fiction film Terminator Salvation (2009);[34] she replaced Claire Danes in the role of Kate Connor.

[34][38] The Guardian described Howard's role as "winsomely" while The New York Times wrote she "upholds the maternal side of the original Sarah Connor legacy".

[42] The film was a box office hit[46] and drew mixed reviews,[47] though Howard's performance received critical acclaim; Honeycutt lauded her as "the epitome of sensual, feline cunning".

[54] She appeared in Tate Taylor's 2011 film adaptation of Kathryn Stockett's novel The Help, in which she played Hilly Holbrook, a racist socialite who leads a Junior League chapter in 1963 Jackson, Mississippi.

[59] Howard, alongside her father, produced Gus Van Sant's Restless (2011), a dark coming-of-age film about a teenage boy and girl who are engrossed with death.

[69] She portrayed Claire Dearing, the ambitious, accomplished operations manager at the titular theme park who undergoes development during the film.

[70] Howard performed extensive ankle exercises to complete the scenes in which her character runs in high heels through almost three feet (0.91 m) of mud, which she described as "one of the hardest things [she's] ever had to do".

[72][73][74] Rolling Stone described her portrayal as "dynamo" and "nobody's patsy" while the Associated Press wrote; "it is Howard who makes the biggest impact ... her transformation is the most convincing one in a film full of dubious evolutions".

[75][76] The Los Angeles Times and The Atlantic considered Dearing and her use of heels "sexist", while Bustle and Inquisitr labeled Howard's character as a "feminist hero".

[99][100] In 2019, Howard voiced the character Bella in the family drama film A Dog's Way Home, which opened to critical and commercial success.

[101][102] Howard appeared as Elton John's mother Sheila Dwight in the musical biopic Rocketman (2019), which was directed by Dexter Fletcher.

[105][106] Rocketman was a box-office hit and garnered critical acclaim, receiving a nomination for the Golden Globe Award for Best Motion Picture – Musical or Comedy.

[107][108] The Chicago Sun-Times praised Howard for her "finely nuanced work" and CinemaBlend called her performance a "wicked portrayal ... that really ties a film together".

[114] Dads received critical acclaim; Variety wrote; "Howard favors observation over lecture, anecdotes over numbers, showing instead of telling what equally split primary-caregiving looks like in contemporary households" and The Guardian said the film "mixes the platitudinous with the genuinely moving".

[117] Howard referred to the larger Star Wars universe as an asset to storytelling, and sought to maintain character depth and appeal to viewers.

[118] Howard's direction received positive responses; Den of Geek said she "[made] the episode pop" and "knows what makes Star Wars tick".