diff --git a/Sources/PackageLoading/ToolsVersionParser.swift b/Sources/PackageLoading/ToolsVersionParser.swift
index f38e2e4eb07..e3df3d9e0df 100644
--- a/Sources/PackageLoading/ToolsVersionParser.swift
+++ b/Sources/PackageLoading/ToolsVersionParser.swift
@@ -55,11 +55,7 @@ public struct ToolsVersionParser {
             throw ManifestParseError.emptyManifest(path: manifestPath)
         }
 
-        do {
-          return try self.parse(utf8String: manifestContentsDecodedWithUTF8)
-        } catch Error.malformedToolsVersionSpecification(.commentMarker(.isMissing)) {
-          throw UnsupportedToolsVersion(packageIdentity: .init(path: manifestPath), currentToolsVersion: .current, packageToolsVersion: .v3)
-        }
+        return try self.parse(utf8String: manifestContentsDecodedWithUTF8)
     }
 
     public static func parse(utf8String: String) throws -> ToolsVersion {
@@ -645,8 +641,16 @@ extension ManifestLoader {
         do {
             regularManifestToolsVersion = try ToolsVersionParser.parse(manifestPath: regularManifest, fileSystem: fileSystem)
         }
-        catch let error as UnsupportedToolsVersion where error.packageToolsVersion == .v3 {
-          regularManifestToolsVersion = .v3
+        catch let error as ToolsVersionParser.Error {
+            // If we have version-specific manifests, there are still more checks we must do if
+            // the error being thrown is that of a missing comment marker.
+            // Set the tools version to 3.1.0 since earlier packages default to this.
+            if case .malformedToolsVersionSpecification(.commentMarker(.isMissing)) = error,
+               !versionSpecificManifests.isEmpty {
+                regularManifestToolsVersion = .v3
+            } else {
+                throw error
+            }
         }
 
         // Find the newest version-specific manifest that is compatible with the current tools version.
diff --git a/Tests/PackageLoadingTests/ToolsVersionParserTests.swift b/Tests/PackageLoadingTests/ToolsVersionParserTests.swift
index c7c6b05778d..96c96d1c330 100644
--- a/Tests/PackageLoadingTests/ToolsVersionParserTests.swift
+++ b/Tests/PackageLoadingTests/ToolsVersionParserTests.swift
@@ -369,6 +369,26 @@ final class ToolsVersionParserTests: XCTestCase {
         }
     }
 
+    /// Verifies that the correct error is thrown for each Swift tools version specification missing entirely.
+    func testMissingSwiftToolsVersion() throws {
+        let manifestSnippetsWithoutVersionSpecifier = "\n import PackageDescription"
+
+        // TODO bp update comments here, as this was copied from above test
+        XCTAssertThrowsError(
+            try self.parse(manifestSnippetsWithoutVersionSpecifier),
+            "a 'ToolsVersionParser.Error' should've been thrown, because the version specifier is missing from the Swift tools version specification"
+        ) { error in
+            guard let error = error as? ToolsVersionParser.Error, case .malformedToolsVersionSpecification(.commentMarker(.isMissing)) = error else {
+                XCTFail("'ToolsVersionLoader.Error.malformedToolsVersionSpecification(.versionSpecifier(.isMissing))' should've been thrown, but a different error is thrown")
+                return
+            }
+            XCTAssertEqual(
+                error.description,
+                "the manifest is missing a Swift tools version specification; consider prepending to the manifest '\(ToolsVersion.current.specification())' to specify the current Swift toolchain version as the lowest Swift version supported by the project; if such a specification already exists, consider moving it to the top of the manifest, or prepending it with '//' to help Swift Package Manager find it"
+            )
+        }
+    }
+
     /// Verifies that the correct error is thrown for each misspelt comment marker in Swift tools version specification.
     func testMisspeltSpecificationCommentMarkers() throws {
         let manifestSnippetsWithMisspeltSpecificationCommentMarker = [
@@ -837,4 +857,42 @@ final class ToolsVersionParserTests: XCTestCase {
         try version.validateToolsVersion(currentToolsVersion, packageIdentity: .plain("lunch"))
         XCTAssertEqual(version.description, "5.0.0")
     }
+
+    func testMissingToolsVersionManifest() throws {
+        let fs = InMemoryFileSystem()
+        let root = AbsolutePath("/pkg")
+
+        // First, test the missing comment marker with the latest tools version.
+        try fs.writeFileContents(root.appending("Package.swift"), string: "\n import PackageDescription")
+        XCTAssertThrowsError(
+            try ManifestLoader.findManifest(packagePath: root, fileSystem: fs, currentToolsVersion: .current)
+        ) { error in
+            guard let error = error as? ToolsVersionParser.Error, case .malformedToolsVersionSpecification(.commentMarker(.isMissing)) = error else {
+                XCTFail("'ToolsVersionParser.Error.malformedToolsVersionSpecification(.commentMarker(.isMissing))' should've been thrown, but a different error is thrown.")
+                return
+            }
+
+            XCTAssertEqual(
+                error.description,
+                "the manifest is missing a Swift tools version specification; consider prepending to the manifest '\(ToolsVersion.current.specification())' to specify the current Swift toolchain version as the lowest Swift version supported by the project; if such a specification already exists, consider moving it to the top of the manifest, or prepending it with '//' to help Swift Package Manager find it"
+            )
+        }
+
+        // Next, test the missing comment marker with tools version .v4. This should default to using 3.1.0.
+        try fs.writeFileContents(root.appending("Package.swift"), string: "\n import PackageDescription")
+        XCTAssertThrowsError(
+            try ManifestLoader.findManifest(packagePath: root, fileSystem: fs, currentToolsVersion: .v4)
+        ) { error in
+            guard let error = error as? UnsupportedToolsVersion, error.packageToolsVersion == .v3 else {
+                XCTFail("'UnsupportedToolsVersion' should've been thrown, but a different error is thrown.")
+                return
+            }
+
+            XCTAssertEqual(
+                error.description,
+                "the manifest is missing a Swift tools version specification; consider prepending to the manifest '\(ToolsVersion.current.specification())' to specify the current Swift toolchain version as the lowest Swift version supported by the project; if such a specification already exists, consider moving it to the top of the manifest, or prepending it with '//' to help Swift Package Manager find it"
+            )
+        }
+    }
+
 }