Because many other colleges have attracted Welsh students at various times, Jesus College is perhaps most accurately described as the 'major Welsh college' at Oxford. Its founding charter contains no provision that the majority of its students, or indeed any of them, should be Welsh. Yet, between 1571 and 1915, an almost unbroken succession of 24 Principals of Jesus came from Wales or were of Welsh descent (interrupted by only one non-Welshman, the Cornish-born Principal Francis Howell from Exeter College, during the late Commonwealth years, 1657-1660). Most College Fellows, until the University reforms of 1859 and later, were also Welsh. During the College's first twenty years, the student body was between one-third and one-half English; but by 1600 it had become much more uniformly Welsh, with only a sprinkling of English students, mainly from the border counties.

Benefactions from well-wishers or old members of the College, who were usually of Welsh descent, endowed a number of fellowships and scholarships, often stipulating that the recipients should be of the benefactors' own kin or belong to their particular parish, county, school, or region in Wales. Eligibility was established, in many cases, by pedigree rather than by academic merit alone. Fellowships (or, from the late 19th century, scholarships) for Channel Islanders, which King Charles I established at Jesus, Exeter and Pembroke Colleges in 1635, and a steady trickle of local Oxford boys entering the College as undergraduates, provided the main geographical variation until the intake broadened after the 19th-century reforms.

Throughout the 17th and early 18th centuries the College had represented the whole Welsh social spectrum, from wealthy landowners' sons enjoying a high standard of comfort to poor boys financing their studies as servitors, with set duties to perform around the College. From the mid- to late 18th century onwards, sons of the richer Welsh gentry tended to go to more fashionable colleges, while many men from relatively humble backgrounds, such as hill farmers' or miners' sons, came to Jesus from the various Welsh endowed schools and (later) County Schools, in many cases gaining financial support from scholarships and exhibitions.

Although the mid-19th-century University reforms ended the specific restrictions attached to many fellowships and scholarships, the College continued to recruit generously from Welsh schools, and also from among graduates of the new university colleges of Wales. Most of these latter took a second BA degree when at Oxford. In recognition of its long-standing Welsh links, the reformed College offered competitive Welsh scholarships and exhibitions to those who had been born or educated in Wales, or could claim at least one Welsh-born parent. After changes in the admissions system, these were merged with the Meyricke scholarships and exhibitions, the outcome of an early 18th-century endowment which had originally favoured North Welshmen. Now awarded (like other scholarships and exhibitions) for promising undergraduate work, these are subject to the same general limitations as the former Welsh awards, with a knowledge of Welsh as an additional qualification.

No evidence exists of the extent to which Welsh was spoken (if at all) in College, although the earliest domestic servants were Welsh and presumably kept up the language, at least among themselves. Official college records were mainly written in Latin; while the College statutes, effective from 1622, forbade public conversation, in class, hall and even the quadrangles, in any language but Latin, Greek or Hebrew. Perhaps in recognition of future clergymens' duties in purely Welsh-speaking areas, Welsh Bibles, grammars and 'other bookes' appeared as items of College expenditure in the 1630s. Yet, within a century of this, when the College purchased seven livings for former fellows (to add to the four Welsh and five English livings that it held through benefactions), these were all in England, within easy riding distance of Oxford. Chapel services in Welsh were held regularly only from the mid-nineteenth century onwards, when Welsh underwent its first serious scholarly revival. The University Professorship of Celtic, known as the Jesus Professorship, has been based in the College since its inception. The first elected Professor (1877-1915) was the distinguished Celtic scholar Sir John Rhys, a Jesus graduate from a humble North Welsh background, later (1895-1915) College Principal.