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Grace garnered further recognition for playing younger versions of characters in I, Tonya (2017), The Haunting of Hill House (2018) and Captain Marvel (2019), and for her lead roles in The Bad Seed (2018), Troop Zero (2019), and Annabelle Comes Home (2019). For playing the abused teenager Esther Keyes in The Handmaid's Tale (2021–2022), Grace was nominated for the Primetime Emmy Award for Outstanding Guest Actress in a Drama Series, making her the first child recognized for a guest acting Emmy. She portrayed Phoebe Spengler in the supernatural comedy films Ghostbusters: Afterlife (2021) and Ghostbusters: Frozen Empire (2024), receiving critical praise and a Critics' Choice Super Award nomination. In 2022, Grace wrote, executive produced, and starred in The Bad Seed Returns, and portrayed Jan Broberg in A Friend of the Family. She then starred in the romantic drama Regretting You (2025), the supernatural horror Five Nights at Freddy's 2 (2025) and the slasher Scream 7 (2026).

After signing with Photo Finish Records in 2020, Grace released her debut single, "Haunted House", in 2021, as part of the Ghostbusters: Afterlife soundtrack. She released two extended plays in 2023: Bittersweet 16 and Autumn Leaves, which explored pop rock and folk sounds, respectively.