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In mid-2007 he starred as the love interest of pop/R&B singer Fergie in the music video for "Big Girls Don't Cry".
In 2008, he starred as a medical student in the horror film Pathology.
He has guest starred on such television series as CSI: Crime Scene Investigation, Sabrina, the Teenage Witch, Law and Order: Special Victims Unit and Boston Public.
He had the part of the main character, Jed Perry, in the short-lived Fox TV series, Opposite Sex, which originally aired in 2000.
From 2001 to 2004, Ventimiglia played brooding teen Jess Mariano on Gilmore Girls; he was introduced in the second season as a main cast member.
He signed on for a spin-off of Gilmore Girls called Windward Circle which was to be focused on the relationship between Jess and his estranged father (played by Rob Estes), but the proposed series never made it to air.
Ventimiglia also produced and developed a mini web-series called It's a Mall World as part of a marketing campaign for American Eagle Outfitters in 2007.He starred as Peter Petrelli on NBC's Heroes from 2006 to 2010, for which he received nominations for Teen Choice, Saturn and People's Choice Awards.He also had roles in the horror films Pathology (2008) and Kiss of the Damned (2013).Ventimiglia later appeared in television as Ian Mitchell on the Crackle original series Chosen as well as Sean Bennigan on The Whispers in 2015.
He reprised his role as Jess Mariano on Netflix's reunion miniseries, Gilmore Girls: A Year in the Life (2016), and currently stars as Jack Pearson on NBC's This Is Us (2016–present).
Ventimiglia, Cundiff, and Divide Pictures partnered with Top Cow to produce the comic series REST which will be a monthly limited series.