The fact that almost nobody in the history of the church has espoused an ongoing apostolate rightly gives us pause. However, we have to do more than poll the great theologians: we have to look at their arguments. After reviewing the main arguments from the history of Reformed theology, I’m persuaded that the supposed link between apostolicity and inspiration/canonicity is inconsistent with a truly Reformed doctrine of Scripture. If you believe that Scripture is self-authenticating, the whole motivation for finding a criterion of inspiration/canonicity drops.
Calvin on apostles
I don’t pretend to give a full and balanced present of Calvin’s polity here, but I would like to point out that he (a) does not essentially link apostolicity to inspiration or resurrection-witness and therefore (b) is open to the possibility of contemporary apostles.
Calvin describes the function of apostles as preaching the gospel far and wide, and planting churches. Speaking of apostles, Calvin writes “Their office was to spread the doctrine of the gospel throughout the whole world, to plant churches, and to erect the kingdom of Christ.” And elsewhere:
The nature of the apostles’ function is clear from this command: “Go, preach the gospel to every creature” [Mark 16:15]. No set limits are allotted to them, but the whole earth is assigned to them to bring into obedience to Christ, in order that by spreading the gospel wherever they can among the nations, they may raise up his Kingdom everywhere. Accordingly, Paul, in desiring to prove his apostleship, recalls that he did not gain any one city for Christ but propagated the gospel far and wide, and did not put his hands to another man’s foundation but planted churches where the name of the Lord was unheard [Rom. 15:19-20]. Apostles, then, were sent out to lead the world back from rebellion to true obedience to God, and to establish his Kingdom everywhere by the preaching of the gospel, or, if you prefer, as the first builders of the church, to lay its foundations in all the world [I Cor. 3:10].
Calvin does not link apostolicity essentially with revelation-reception or seeing the risen Christ. This makes him open to the possibility of present-day apostles. Speaking of the apostles, prophets, evangelists, pastors, and teachers mentioned by Paul in Eph. 4:11, Calvin writes, “Of these only the last two have an ordinary office in the church; the Lord raised up the first three at the beginning of his Kingdom, and now and again revives them as the need of the times demands.”
According to this interpretation (which seems to me to be in agreement with both the words and opinion of Paul), these three functions [apostle, prophet, evangelist] were not established in the church as permanent ones, but only for that time during which churches were to be erected where none existed before, or where they were to be carried over from Moses to Christ. Still, I do not deny that the Lord has sometimes at a later period raised up apostles, or at least evangelists in their place, as has happened in our own day. For there was need for such persons to lead the church back from the rebellion of Antichrist. Nonetheless, I call this office “extraordinary,” because in duly constituted churches it has no place.
In a footnote to the sentence “Still, I do not deny…,” editor John T. McNeill says that Calvin is “Referring chiefly to Luther, whom he elsewhere often praises. Cf. Calvin’s Defensio adversus Pighium, where Luther is called ‘a distinguished apostle of Christ by whose ministry the light of the gospel has shone’ (CR VI. 250).”
For Calvin, it is the word, not an ecclesiastical office, which is inspired. One might expect Calvin to polemicize against the papacy by announcing that since the apostolate has ceased, there can be no pope. But this is not how he argues. Instead he says
In truth, he [Paul] plainly rejects it [the papacy] as without foundation, when he ascribes superiority to Christ alone, and represents the apostles, and all the pastors, as indeed inferior to Him, but associated on an equal level with each other.
The apostolate, biblically understood, was not a “temporary papacy” but in fact undermines the pretensions of the papacy. Apostles and pastors are “associated on an equal level with one another.” Calvin always stresses that it is the apostolic message, not the apostolic office, which is the foundation of the church (see e.g. his commentary on Eph. 2:20). Consistency with the divine word gives authority to ecclesiastical offices, but the divine word does not need to be validated by any ecclesiastical office, even the highest. I think that this is Calvin’s point in his commentary on Gal. 1:8:
[Paul] demands such unhesitating belief of his preaching, that he pronounces a curse on all who dared to contradict it.
And here it is not a little remarkable, that he begins with himself; for thus he anticipates a slander with which his enemies would have loaded him. “You wish to have everything which comes from you received without hesitation, because it is your own.” To show that there is no foundation for such a statement, he instantly surrenders the right of advancing anything against his own doctrine. He claims no superiority, in this respect, over other men, but justly demands from all, equally with himself, subjection to the word of God.
One might think that Calvin is only saying that Paul demands the reception of his message not because it is Paul’s, but because it is apostolic. This construal keeps the apostolic office per se infallible. But Calvin’s commentary on Gal. 2:11 overthrows this reading. Calvin emphasizes the fact that even Peter, an apostle, can be rightly rebuked. Consider what he makes of this fact: “This is another thunderbolt which strikes the Papacy of Rome. It exposes the impudent pretensions of the Roman Antichrist, who boasts that he is not bound to assign a reason, and sets at defiance the judgment of the whole Church.” Calvin’s point here is that if Peter, qua apostle, can be tested against the divine word and found wanting, then so too can any ecclesiastical official.
In Institutes IV.viii, “The Power of the Church with Respect to Articles of Faith; and How in the Papacy, with Unbridled License, the Church has been Led to Corrupt All Purity of Doctrine,” Calvin stresses that OT prophets, priests, apostles, and pastors are all on a level with respect to their doctrinal authority: all are constrained to preach and teach only what they have received by revelation. Whether or not they are first recipients of a revelation (prophets and apostles), or secondary recipients who proclaim it (teachers and pastors) makes no difference as far as their inherent authority goes. We cannot put implicit faith in any person, apostolic or otherwise:
As far as individual men are concerned, by the Lord, Paul was surely ordained apostle to the Corinthians, but he denies that he has dominion over their faith [II Cor. 1:24]. Now who would dare claim a dominion that Paul attests does not belong even to him? But if he had recognized such license to teach that a shepherd could by right require men to subscribe with unquestioning faith to all that he might teach—he would never have communicated to these same Corinthians the regulation that when two or three prophets speak “let the others discriminate. But if revelation is made to another sitting by, let the first be silent.” [I Cor. 14:29-30 p.]. For he thus spared no one, and subjected the authority of all to the judgment of God’s Word.
One of the great principles of the Reformation is that the church is founded on the word, but the word is not founded on the church. The principle is epistemic: we recognize the true church as that which truly preaches the word, but our recognition of the divine word does not depend upon the authority of church councils or popes or even miracles or whatever. It seems to me that the later Reformed and evangelical tradition gives up this principle just to the extent that it makes apostolicity a criterion for inspiration and canonicity. The sanction of an apostle is neither necessary nor sufficient for recognizing the self-authenticating word as such. I think that this is what is behind Calvin’s uncoupling of apostolicity and the authority of the word.
Several prominent Reformed theologians after Calvin make the office of apostle (and of prophet, but I leave that aside now) inerrant, and yolk it to inspiration and canonicity.
Zacharias Ursinus writes that “Apostles were ministers called immediately by Christ…having a similar testimony from God that they could not err in the doctrine.”
The ordering of chapters 23-25 of Book One of William Ames’ The Marrow of Theology are telling indicators of his theology of the apostolate. Between chapter 23, “The Extraordinary Ministers of the Church,” and chapter 25, “Ordinary Ministers and Their Office in Preaching,” intervenes chapter 24, “Holy Scripture.”
Extraordinary ministers “always have extraordinary gifts and assistance so that they minister without error,” and “the calling to such a ministry is direct.” These ministers are organs of revelation. Miracles are not necessary for the confirmation of their messages, nor are they sufficient, but they are sometimes “added for more abundant confirmation.”
33. This extraordinary ministry is either for the first instituting of a church, or for the special and extraordinary conservation of a church, or for the extraordinary restoring of a church which has collapsed.
34. The ministry of instituting a church is always accompanied by a testimony of miracles. Heb. 2:3, 4…”
“37. The prophets, apostles, and evangelists were extraordinary ministers” but the Reformers were not, strictly speaking.
Naturally, chapter 24, “Holy Scripture,” begins by noting that extraordinary ministers were raised up for the purpose of delivering, orally and in writing, divine revelation. “Only those could set down the rule of faith and conduct in writing who in that matter were free from all error because of the direct and infallible direction they had from God.”
Richard Baxter writes that it would be inconsistent with the faithfulness of God to allow apostles to err.
Yet if any of the commissioners do err in their own particular conversations, [footnote: As Peter, Gal. ii. 12, 13] or in matters without the extent of their commission, this may consist with the faithfulness of God: God hath not promised them infallibility and perfection; the disgrace is their own: but if they should miscarry in that wherein they are sent to be a rule to others, the church would then have an imperfect rule, and the dishonor would redound to God.
Francis Turretin also develops this distinction between errors of doctrine (which are impossible for apostles) and errors in conduct (which are possible). “The apostles were infallible in faith, not in practice…The dissimulation and hypocrisy of Peter (Gal. 2:12) was a sin of life, not an error of faith.”
James Bannerman argues that the apostolic office was “extraordinary and temporary” rather than “ordinary and permanent.” First, the apostles were appointed to be eye-witnesses of the resurrection, and there are of course no longer any such witnesses. He cites here the criteria of Judas’ replacement (Acts 1:21ff.), and notes that Paul’s witnessing of the risen Christ receives great emphasis. Second, the apostles were directly called by Christ himself. Thirdly, the apostles were uniquely endowed with “supernatural power which they possessed to qualify them for their extraordinary mission.” It was requisite that the apostles be inspired, “teachers of infallible truth,” and also that they have miraculous powers to accredit their teaching. The gift of tongues was given to them so that they might speak the gospel to foreigners and thus to all nations. “The powers of inspiration, of miracles, and of tongues are spoken of by Paul as ‘the signs of an apostle’…–marking out the authority and the special character of his office.” The apostolic office exercised “an absolute authority” and was “invested with an infallible power to teach.” Fourth, the apostles had a “universal commission and unlimited authority.”
B.B. Warfield states that the criterion for canonicity is “imposition by the apostles as ‘law’”.
Reflections on the development of the Reformed doctrine of the apostolate.
The main point I want to make here is that the Reformed stress on the inerrancy (and hence temporariness) of the apostolate seems to happen at the same time as the decline of the Reformed doctrine of the self-authentication of Scripture. If Scripture is self-authenticating, then you simply don’t need a criterion of inspiration/canonicity over and above Scripture itself. But if Scripture is not self-authenticating, then you do need such a criterion. And since early in church history, the church has latched onto apostolicity in one form or another as the criterion. The apostolic criterion of canonicity is most at home in an evidentialist apologetic. The evidentialist must provide a criterion for inspiration. Ultimately, that criterion will be miracles, but miracles will then be linked to the apostolate in some essential way such that the closing of the canon implies the cessation of miracles and the apostolate (and vice versa). Naturally, we find Norman Geisler saying that non-apostolic NT authors that “each of these had his message confirmed by the twelve apostles.” And naturally, as we find the Reformed stressing the foundational significance of the indicia of Scripture rather than its autopistia, we find them stressing apostolicity as a criterion of canonicity. On the other hand, you will search in vain for the apostolic criterion in John Owen’s magnificent The Divine Original of Scripture, because Owen has such a robust notion of the self-authentication of Scripture. He does not need a criterion of inspiration and canonicity, because Scripture is self-evidencing.
The tension between the self-authentication of Scripture and the apostolicity-canonicity link is also evident in Herman Ridderbos. Ridderbos argues that the NT does substantially support Warfield’s apostolic criterion. However, Ridderbos acknowledges the impossibility of proving that all of the NT books meet the criterion. Ridderbos maintains the connection between inspiration and apostolicity, but inverts the evidentialist strategy. He argues that because the NT books are self-authenticating, we know that they are inspired; therefore, we can infer that all of the books are tied to an apostle.
It may seem like Ridderbos’ approach accomplishes precious little, since it has no evidential value for those who do not already believe in the NT canon. But, if you could show on independent grounds that the apostolate has ceased, then you would have a fine argument for the closing of the canon of Scripture in the first century. You could rule out e.g. the Book of Mormon. In order to make this argument tight, you have to deny that the prophets of Eph. 2:20/3:5 are NT prophets, or else mount an independent argument for the cessation of inspired NT prophecy. The reason is that the prophets of Eph. 2:20/3:5 seem to be giving inspired revelation. If such prophets might still be operative, then it seems that there might still be inspired (and canonical) revelation forthcoming. But in any case, once you’ve already thrown yourself upon the self-authentication of Scripture (as Ridderbos rightly does), you don’t need another argument for the closing of the canon. No other self-authenticating, God-breathed word has come forth. This coheres with our general expectation that the climax of God’s redemptive acts and of his redemptive words should coincide.
So, from a historical and systematic perspective, I think the essential link between apostolicity and inspiration/canonicity is useless, groundless, and artificial.
 John Calvin, Commentaries on the Epistles of Paul to the Galatians and Ephesians, trans. William Pringle (Edinburgh, Scotland: Calvin Translation Society, n.d.; reprinted, Grand Rapids, Mich.: Baker, 2005) 279
 Institutes of the Christian Religion 4.3.4, 1056-57
 Institutes of the Christian Religion 4.3.4, 1056
 Institutes of the Christian Religion 4.3.4, 1057
 Institutes of the Christian Religion 4.3.4, 1057n4
 John Calvin, Commentaries on the Epistles of Paul to the Galatians and Ephesians, trans. William Pringle (Edinburgh, Scotland: Calvin Translation Society, n.d.; reprinted, Grand Rapids, Mich.: Baker, 2005) 280-281
 The Commentary of Dr. Zacharias Ursinus on the Heidelberg Catechism , trans. G.W. Willard (Columbus, OH: Second American edition, 1852; reprinted, Phillipsburg, NJ: Presbyterian & Reformed, n.d.) 572
 Ed. John D. Eusden (Grand Rapids, Mich.: Baker, 1997)
 183 (point 25), 184 (point 27).
 185 (point 35), citing Deut. 13:1-3 and Gal. 1:8.
 Richard Baxter, The Saints’ Everlasting Rest (Fearns, Great Britain: Christian Focus Publications, 1998) 143.
 Francis Turretin, Institutes of Elenctic Theology, translated by George Musgrave Giger, edited by James T. Dennison, Jr. (Phillipsburg, NJ: Presbyterian & Reformed, 1992) 2.4.24, vol. 1 p. 69.
James Bannerman, The Church of Christ, 2 vols (New York: Westminster Publishing House, n.d.) 217
 Warfield, “The Canon of the New Testament” in The Inspiration and Authority of the Bible,415. Thus also Norman Geisler Christian Apologetics 369.
 Christian Apologetics 369. So also Warfield, “The Canon of the New Testament” 415. I can’t find any discussion of the canon in Classical Apologetics.
 John Owen, The Divine Original of the Scripture, in The Works of John Owen, vol. XVI, ed. William H. Goold (First published by Johnstone & Hunter, 1850-1853; reprinted, Carlisle, Penn.: The Banner of Truth Trust, 1968, 1995)
 Herman N. Ridderbos Redemptive History and the New Testament Scriptures, translated by H. De Jongste, revised by Richard B. Gaffin Jr., 2nd rev. ed. (Phillipsburg, NJ: Presbyterian & Reformed, 1988). Wayne Grudem takes a similar approach in his Systematic Theology.
 Ridderbos does add his own important details. He argues that apostolic tradition can be farther removed from the actual person of the apostle than Warfield seems to envision.