Cusack began acting in films in the early 1980s. His first on screen appearances was in minor roles, Class (1983) and John Hughes directorial debut film Sixteen Candles (1984). On the set of Grandview, U.S.A. (1984), his co-star Jamie Lee Curtis gifted Cusack with his first car, a 1974 Chevrolet Impala, which she had named 'La Bamba'. 16-year-old Cusack made his breakthrough performance in Rob Reiner's teen comedy The Sure Thing (1985). It was a critical success, but has since become an underrated film.

He then took on the small-town teen dark comedy film Better Off Dead (1985). Cusack was initially embarrassed and disappointed by the film, describing it as the "worst thing he had ever seen" on his first watch. The film had a budget of $3 million and grossed $10.3 million at the box office, but the studio still considered it a failure. Cusack also worked with the director Savage Steve Holland on One Crazy Summer (1986).

Cusack then had a brief appearance in Rob Reiner's Stand by Me (1986) as the older brother of Gordie, a film based on Stephen King's The Body. On the film, co-star Kiefer Sutherland recalled, "John Cusack was on the film for at least a week. I admired what he was doing and thought he was an actor I wanted to emulate." In 1988, Cusack went on and starred in the Independent film Eight Men Out (1988), about Major League Baseball's Black Sox Scandal during the 1919 World Series. He also appeared in the cult comedy Tapeheads (1988), a film by executive producer Michael Nesmith.

In the late 1980s, Cusack starred in Cameron Crowe's directorial debut film, Say Anything... (1989). He starred opposite actress Ione Skye, playing the title character Lloyd Dobler who experiences a romance with Diane Court (Skye). Cusack was reluctant to do the film at first, but he gave his character dimension through referencing the English punk band The Clash, and The Replacements. In the film, Cusack became known for the infamous boombox scene, in which his character Lloyd stands near Diane's bedroom window, and wordlessly holds up a cassette player above his head, blasting Peter Gabriel's 1986 song "In Your Eyes". His character Lloyd Dobler had since inspired popular culture, such as the band Lloyd Dobler Effect, and Frank Iero's band Pencey Prep with their misspelled song "Lloyd Dobbler".
In the 1990s, Cusack played a con artist in Stephen Frears' 1990 neo-noir film The Grifters. He then appeared in a series of independent films such as True Colors (1991), and Money for Nothing (1993). In the Quentin Tarantino cult classic film, Pulp Fiction (1994), the role of Lance was originally written with Cusack in mind, however, the part went to Eric Stoltz.

After …

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Cusack is anti-war, having tweeted, "Being anti-war — is pro-troops — pro-human". Between 2005 and 2009, Cusack wrote blogs for The Huffington Post, which included an interview with Naomi Klein. He voiced his opposition to the war in Iraq and Bush's administration, calling the government's worldview "depressing, corrupt, unlawful, and tragically absurd". He also appeared in a June 2008 MoveOn.org advertisement, where he said that George W. Bush and John McCain had the same governing priorities.

Cusack criticized the Obama administration for its drone policy in the Middle East and its support of the National Defense Authorization Act, and became one of the initial supporters of the Freedom of the Press Foundation in 2012. In June 2015, he stated in an interview with The Daily Beast that "when you talk about drones, the American Empire, the NSA, civil liberties, attacks on journalism and whistleblowers, [Obama] is as bad or worse than Bush". He later criticized the publication for misquoting him in order to make an interesting headline.

In 2015, Cusack, Daniel Ellsberg and Arundhati Roy met Edward Snowden, who had fled the US because of his leaks of classified information surrounding illegal population surveillance, at a Moscow hotel room. This meeting was converted into a book co-authored with Roy titled Things That Can and Cannot Be Said.

Cusack endorsed Senator Bernie Sanders in his 2016 and 2020 presidential bids. He is a member of the Democratic Socialists of America.

During May 2020, Cusack was recording a George Floyd protest in Chicago on social media when he was attacked by police with batons and later pepper-sprayed.

I would love to think about other things—poetry, love, anything else. But that’s just not the times we’re in. And, y’know, not all anger is just sort of somebody stuck in some rut in a basement. If you can’t be outraged on behalf of other people, or express anger at injustice, maybe that is its own rut. Sure, I might go too far sometimes. But I really just want to get across the message: that we’re sleepwalking into an incredibly dark possible future. Maybe being outspoken hurts your career… I’m just aware it helps me sleep better at night, knowing that I wasn’t passive during this time.— John Cusack, The Guardian (October 4, 2020)
Cusack has been fiercely critical of Israel's military actions against Palestinians. He criticized Israel's killing of Palestinians in the 2014 Gaza War, retweeting for weeks articles supporting Gaza. Cusack signed an open letter in support of Lorde cancelli…

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Cusack trained in kickboxing under former world kickboxing champion Benny Urquidez for over 20 years. He began training under Urquidez in preparation for his role in Say Anything... and holds the rank of a level six black belt in Urquidez's Ukidokan Kickboxing system.

In March 2008, police arrested Emily Leatherman outside Cusack's Malibu, California, home for stalking him. On October 10, 2008, Leatherman pleaded no contest and received five years' probation and mandatory psychiatric counseling, and was ordered to stay away from Cusack, his home, and business for the next 10 years.