Summer's career began in 1983 when she was cast as the voice of niece Penny on the original cartoon version of Inspector Gadget. Her unique, throaty voice was instantly recognizable to casting agents (as well as viewers even today), who began frequently casting her in animated programs. Many of these were part of cult franchises, like The Care Bears Movie (1985) and Ewoks (1985, part of the Star Wars franchise).

Audiences finally had a chance to put Summer's voice to a face when she was cast as the afrocentric Winifred "Freddie" Brooks in the Cosby Show spin-off A Different World. Summer, a multiracial woman (of Caucasian, Black, and Native American descent) who wears her hair in a large afro-style, proved to have an appearance as unique as her voice. She remained a regular cast member of the show from 1988 to 1993.

During the run of A Different World Summer continued working in voice acting. She was cast in the short-lived television series Sweet Justice in 1994; it went off air in 1995. Barring numerous guest appearances on other live action television shows such as Living Single and The Fresh Prince of Bel-Air, Summer's professional work since has been limited to voice acting.

In all, Summer has voiced over 70 animated characters between 1983 and 2004. These have spanned the realm of video games, cartoon television series, animated films and commercials. Among her most famous roles was in Tiny Toon Adventures (1990) as Elmyra Duff and in Sonic the Hedgehog as Dulcy the dragon. Among her more recent roles are Susie Carmichael in All Grown Up! (itself a role carried over from Rugrats), and the Lincoln sisters Abby/Numbuh 5 and Teen Ninja Cree (formerly Numbuh 11) in Codename: Kids Next Door. She also does voices in M&M's advertisements as the voice of the female green M&M.

Summer has also ventured into the realm of music. In 1993 she released an album (as lead singer) with her band Subject to Change. The album was not officially released by Capitol Records because of creative differences; the records that were produced were distributed promotionally and are considered a rarity. The band, with an aggressive political message and rock-soul fusion sound, remained popular as a co-headlining act with other performers. In 1999 Summer released the solo album Street Faerie produced by and featuring guest artist (and friend) Lenny Kravitz, the album was not hugely successful. Summer toured as Kravitz's opening act, but her label dropped her and a planned spot with Lillith Fair was cancelled. The label continued to promote it, however, sending out a four track sampler to radio and issuing remix singles of the track "Revelation Sunshine" in Australia and Europe. Her musical talent may have had an influence on Summer's portrayal of Susie as a "singer with real talent" . She is also known for voicing the Summoner Belgemine and young Tidus in the video game blockbuster Final Fantasy X, and the Summoner Lenne from Final Fantasy X-2. She is also well know for the role of Tandi from Fallout 1 and 2.

Since 2004, Cree has been a cast member of Comedy Central's animated series Drawn Together, providing the voice of Foxxy Love, a sexually promiscuous spoof of Josie and the Pussycats' Valerie Brown as well as 1970s blaxploitation characters. Summer also provides many of the series's guest voices, having played Strawberry Sweetcake, Ni-Pul, and a number of others. In Danny Phantom (2004), she also provided the voice of Valerie Gray, a ghost hunter. In 2005, she added the voice of some Squirrel Scouts to her character credits on Cartoon Network's Joe Murray-created and produced series Camp Lazlo, as well as that of Rayna, the best friend of the titular character in the Disney cartoon The Buzz on Maggie. In 2006, she added the voice of Mrs. Tusk in the Cartoon Network series My Gym Partner's a Monkey to her list of credits.