From 2009 to 2020, he portrayed Mitchell Pritchett on the sitcom Modern Family, for which he earned five consecutive nominations for the Primetime Emmy Award for Outstanding Supporting Actor in a Comedy Series.

He has appeared in numerous productions of Shakespeare in the Park, acting in A Midsummer Night's Dream (2007), A Winter's Tale (2010), The Merchant of Venice (2010), and The Tempest (2015).

[10] In New York City, Ferguson worked mainly in Off-Broadway and Broadway theatre, including the Tony Award-winning The 25th Annual Putnam County Spelling Bee, where he originated the role of Leaf Coneybear.

In March 2012, Ferguson was featured as Dr. Ilan Meyer in a performance of Dustin Lance Black's play 8, a staged reenactment of Perry v. Brown, the federal trial that overturned California's Proposition 8 ban on same-sex marriage.

[12] The production was held at the Wilshire Ebell Theatre and broadcast on YouTube to raise money for the American Foundation for Equal Rights, a non-profit organization funding the plaintiffs' legal team and sponsoring the play.

For his performance, Ferguson has received five consecutive Emmy Award nominations for Outstanding Supporting Actor in a Comedy Series.

[22] In January 2013, the couple were recruited by Lieutenant Governor of Illinois Sheila Simon to lobby legislators to pass SB10 which would allow same-sex marriage.

[27] He participated heavily in the ACLU's "Out for Freedom" campaign[28][29] They noted that Ferguson travelled to New Mexico, his home state, to take part in same sex marriage efforts.

[28] In November 2013, a pop-up retail store for 'Tie The Knot' was located at the Los Angeles Beverly Center featuring the fourth collection from the couple,[31] including professional athlete designs with Scott Fujita and Chris Kluwe, and Brittney Griner.