The agencies - which are to handle consumer PR and trade/technical/B2B PR respectively - will share a PR budget of more than £1m.
Both agencies - which sealed their retained contracts after competitive pitches - report to O2 vice-president marketing Will Harris.
O2 has previously used Edelman PR Worldwide and MacLaurin on consumer projects, in addition to JCPR. Neither Edelman, MacLaurin, nor Fishburn Hedges - which handled B2B and corporate work in O2's days as BT Cellnet - work with O2 any longer.
In addition, Edelman-owned agency PR21 will no longer handle online PR from the end of this month, O2 UK head of press Carole Williams confirmed.
JCPR has also worked with O2 on various projects already this year. In June it handled consumer PR for the launch of O2's xda - a product that combines a phone with a PDA (personal digital assistant).
The agency has also been handling project work for O2's sponsorships of Arsenal Football Club, the Rugby Football Union and music therapy charity Nordoff Robbins.
JCPR has around 15 staff working on the O2 account, with founding partner Robert Phillips overseeing the agency team.
Midnight is tasked with promoting O2's voice services for business - such as Groupworker and Business First.
Around ten Midnight staff are to work on the account, with associate director Antony Mayfield leading the work.
Mayfield said: 'The IT press is very important for O2's story. We will target IT directors, the telecoms press, plus the new media and internet press'.
Edelman PR Worldwide handled the UK launch event for O2 in Europe in May this year, when the firm rebranded from BT Cellnet. JCPR handled European media relations in Germany, Ireland and The Netherlands for that event.
MacLaurin handled consumer PR for the former BT Cellnet and also handled PR for O2's sponsorship of the third series of reality TV show Big Brother earlier this year.
Financial, corporate and investor relations work will continue to be handled by the PR team at O2's parent firm mm02. The Maitland Consultancy is the retained agency in this field.