He made his professional acting debut originating the role of John Blakemore in Sir David Hare's South Downs in the West End.

His other notable work includes his roles in Freak Show, Howards End, Goodbye Christopher Robin, Ghost Stories, The Last Duel and Andor.

[14] Lawther's professional debut came at the age of 16, when he appeared as John Blakemore in Sir David Hare's South Downs at Chichester Festival Theatre.

[19] Subsequently, he appeared in a supporting role as a maths prodigy in the critically acclaimed coming-of-age drama film X+Y, alongside Asa Butterfield and Sally Hawkins.

He returned to the theatre doing various small productions in London during this period, playing a sexually precocious young gay man in The Glass Supper, and the lead in the post-apocalyptic Crushed Shells and Mud.

In 2017, Lawther played Tibby Schlegel in Howards End, a BBC One adaptation of the E.M. Forster novel that starred Hayley Atwell, as well as the lead role of Billy Bloom in Trudie Styler's Freak Show, where he was supported by Bette Midler, Abigail Breslin, AnnaSophia Robb, Lorraine Toussaint and Larry Pine.

He also originated the role of Sam in the Stephen Daltry-directed play The Jungle, which focused on the refugee crisis in Calais, in both its London and New York productions.

Lawther spent time in France meeting with refugees for this job, and ultimately found it to be one of his most challenging roles due to his character's right-wing views which were antithetical to his own.

In 2020, Lawther played the lead role in Régis Roinsard's thriller, Les Traducteurs (The Translators), his first non-English language film.

He starred as Ariel in a French production of Shakespeare's The Tempest at Les Bouffes du Nord directed by Peter Brook and Marie-Hélène Estienne[23] and replaces Andrew Scott in the titular role of Hamlet when Robert Icke's adaptation is brought to New York City, after previously being delayed due to the COVID-19 pandemic.

In 2021, Lawther made his directorial debut with the music video for "Fountainhead" by Linus Fenton, starring Roman Griffin Davis and sponsored by CALM.

[25] In 2022, he wrote and directed the short film For People in Trouble, produced by Ben Affleck and Matt Damon and starring Emma D'Arcy and Archie Madekwe.

[33] After seeing a sixteen-year-old Lawther's West End debut in South Downs, Dame Maggie Smith reportedly remarked to him that "most of us spend our lives trying to do what you've achieved".