During this time, Ingram developed a reputation in the Los Angeles area as a session vocalist, and came to the attention of ex-Motown songwriter and producer Lamont Dozier.

Dozier invited Ingram to contribute vocals to some material; one such song, "Love's Calling," garnered some airplay. The remainder of the material surfaced in 1980 on the album Zingara.

In 1981, Ingram provided the vocals to "Just Once" and "One Hundred Ways" on Quincy Jones's album The Dude. He won a Grammy award for best R&B vocal performance for his work on this album. Ingram's debut album, It’s Your Night, appeared in 1983, including the ballad "There’s No Easy Way." He also worked with other notable R&B artists such as Ray Charles, Anita Baker, Viktor Lazlo, Nancy Wilson, Natalie Cole, and Kenny Rogers. In 1990, he scored a No. 1 hit on the pop charts with the love ballad "I Don't Have the Heart" from his It's Real album.

But Ingram was best known throughout the decade for his hit collaborations. He went to No. 1 on the pop charts with Patti Austin on "Baby, Come to Me," a song made popular on TV's "General Hospital." A second Austin/Ingram duet, "How Do You Keep the Music Playing?" was featured in the movie "Best Friends" and earned an Oscar nomination. A few years later, he won a 1985 Grammy Award for "Yah Mo B There," a duet with Michael McDonald. And he teamed up with Kenny Rogers and Kim Carnes for the Top 40 ballad "What About Me?" in 1984.

In 1987, he teamed with American vocalist Linda Ronstadt, and had a US Pop No. 2 Hit with Somewhere Out There, the theme from the animated feature film, An American Tail. The song garnered Grammy and Academy Award nominations and was certifed gold (over 500,000 U.S. copies sold) by the RIAA.

Ingram performed two solos on the 1985 recording and video of "We Are the World." He also co-wrote "P.Y.T. (Pretty Young Thing)" which was recorded by Michael Jackson on his blockbuster Thriller.

In the 1990s, his highest-profile team-up came again with Quincy Jones, on the song "The Secret Garden." This song also featured vocals by Barry White, El Debarge and Al B. Sure!
Soundtrack songs were popular for Ingram in the 1990s. From the movie Sarafina! came "One More Time," and from City Slickers came "Where Did My Heart Go?" His 1994 composition "The Day I Fell in Love", which he dueted with Dolly Parton, was the theme song for the movie Beethoven's 2nd and was nominated for an Academy Award for Best Original Song.

During the summer of 2006, Ingram participated in the U.S. television reality show Celebrity Duets as a duet partner. The show combined professional vocalists, of different musical genre, with entertainers of different backgrounds in a weekly elimination competition. In 2007, he and neo-soul singer Angie Stone teamed up on "My People."

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