The band was formed by Wendy Robinson (vocals) and Polly Hancock (vocals, guitar), initially with a drum machine. This line-up recorded the debut "Don't Go Back" EP on Big Cat UK (catalogue number BBA02) in August 1988)  achieving "Single of the Week" in Melody Maker. A John Peel session, produced by Dale Griffin and recorded at the BBC studios in Golders Green, London, was first broadcast on 21 September 1988 and repeated on 11 October 1988. It featured four original songs; "Perfect Dream Home", "Fine Lines", "Dr Fell" and "Backward" Daydream. They then recruited Dana Baldinger (b. Seattle, WA), and signed to One Little Indian Records, releasing "Please Let Me Go" as a single in April 1990; this too attained Single of The Week in Melody Maker. Baldinger was eventually replaced by Anne Rogers of The Crowd Scene. In December 1989, the British music magazine NME reported that the Popinjays, along with others such as Power of Dreams, Carter the Unstoppable Sex Machine and The Charlatans, were their pick as 'stars of tomorrow'. 

Their debut album Bang Up To Date With The Popinjays was released in April 1990 and was followed by a live tour in May and June 1990 with One Little Indian label mates Kitchens of Distinction. In the autumn of 1990 Seamus Feeney joined the line up on drums making the band a four-piece for the first time. The band continued with live shows through the autumn, touring with both Cud and The Heart Throbs. The next single Vote Elvis was produced by Jessica Corcoran at The Greenhouse studios in London. In 1991 The Popinjays signed to US Independent label Alpha International and the single Vote Elvis was released in the United States in April 1991 entering the billboard Modern Rock charts the following month peaking at number 17 in June 1991.

In August 1991 the band played at the Reading Festival UK and in December of that year the second album Flying Down to Mono Valley was recorded at The Farmyard with Ian Broudie producing.

On 11 May 1992 the single Monster Mouth was released by One Little Indian records and a UK tour to support the release of the album Flying Down to Mono Valley followed from August through to October 1992.

In 1992 the rhythm section was replaced by two brothers and former members of the band Airhead, namely bassist Ben Kesteven and drummer Sam Kesteven.

In 1994 the third and final album Tales from the Urban Prairie was recorded and released, again on One Little Indian Records. a BBC Radio live session with Mark Radcliffe was broadcast on 1 June 1994.

After a 21-year hiatus, in April 2015 The Popinjays original line up of Wendy Robinson and Polly Hancock played their first live show in 21 years at The Lexington, London on April 4, 2015, and again at Indie Daze at The Forum London on October 3, 2015.