diff --git a/packages/typescript/src/api/proto.generated.ts b/packages/typescript/src/api/proto.generated.ts
index 8a96a261b2fcd..497e292795e2e 100644
--- a/packages/typescript/src/api/proto.generated.ts
+++ b/packages/typescript/src/api/proto.generated.ts
@@ -1339,6 +1339,7 @@ export interface SnapshotRequestChangesParams {
      * tsconfig that contains it; if found, that configured project is loaded and
      * becomes the file's default project. Otherwise the file is loaded into the
      * inferred project (e.g. a node_modules d.ts not in any project's import graph).
+     * If a file cannot be loaded into any project, the request fails.
      */
     openFiles?: readonly DocumentIdentifier[] | undefined;
     /**
diff --git a/packages/typescript/test/async/api.test.ts b/packages/typescript/test/async/api.test.ts
index 04d9a437ab71e..5db333944c527 100644
--- a/packages/typescript/test/async/api.test.ts
+++ b/packages/typescript/test/async/api.test.ts
@@ -6972,6 +6972,47 @@ describe("Program - diagnostics", () => {
 });
 
 describe("getDefaultProjectForFile", () => {
+    test("snapshot opens reject unreadable virtual files without panicking", async () => {
+        const fileName = "/src/App.vue.ts";
+        const source = `export const component = 1;`;
+        const fs = createVirtualFileSystem({
+            "/tsconfig.json": JSON.stringify({ files: ["/src/index.ts"] }),
+            "/src/index.ts": `export const x = 1;`,
+            "/src/App.vue": source,
+        });
+        let virtualFileAvailable = false;
+        await using api = new API({
+            cwd: fileURLToPath(new URL("../../../../", import.meta.url).toString()),
+            fs: {
+                ...fs,
+                readFile: path => virtualFileAvailable && path === fileName ? source : fs.readFile!(path),
+                fileExists: path => virtualFileAvailable && path === fileName ? true : fs.fileExists!(path),
+            },
+        });
+        const snapshot = await api.createSnapshot({
+            openProjects: ["/tsconfig.json"],
+            openFiles: ["/src/index.ts"],
+        });
+
+        const expectedError = /client error: failed to .*snapshot: no project found for opened file: \/src\/App\.vue\.ts/;
+        await assert.rejects(snapshot.update({ openFiles: [fileName] }), expectedError); // @sync: assert.throws(() => snapshot.update({ openFiles: [fileName] }), expectedError);
+        await assert.rejects(api.createSnapshot({ openFiles: [fileName] }), expectedError); // @sync: assert.throws(() => api.createSnapshot({ openFiles: [fileName] }), expectedError);
+
+        virtualFileAvailable = true;
+        const updated = await snapshot.update({ openFiles: [fileName] });
+        const project = await updated.getDefaultProjectForFile(fileName);
+        assert.ok(project);
+        assert.equal(project.configFileName, "");
+        assert.equal((await project.program.getSourceFile(fileName))?.text, source);
+        assert.equal(await snapshot.getDefaultProjectForFile(fileName), undefined);
+        assert.ok(await updated.getConfiguredProject("/tsconfig.json"));
+
+        virtualFileAvailable = false;
+        const reopen = { openFiles: [fileName], fileNotifications: { deleted: [fileName] } };
+        await assert.rejects(updated.update(reopen), expectedError); // @sync: assert.throws(() => updated.update(reopen), expectedError);
+        assert.equal((await project.program.getSourceFile(fileName))?.text, source);
+    });
+
     test("finds inferred project for d.ts in node_modules after openFiles", async () => {
         await using api = spawnAPI({
             "/tsconfig.json": JSON.stringify({ compilerOptions: { strict: true } }),
diff --git a/packages/typescript/test/sync/api.test.ts b/packages/typescript/test/sync/api.test.ts
index d6bae9e4ae241..5c5ca05f7ee32 100644
--- a/packages/typescript/test/sync/api.test.ts
+++ b/packages/typescript/test/sync/api.test.ts
@@ -6840,6 +6840,47 @@ describe("Program - diagnostics", () => {
 });
 
 describe("getDefaultProjectForFile", () => {
+    test("snapshot opens reject unreadable virtual files without panicking", () => {
+        const fileName = "/src/App.vue.ts";
+        const source = `export const component = 1;`;
+        const fs = createVirtualFileSystem({
+            "/tsconfig.json": JSON.stringify({ files: ["/src/index.ts"] }),
+            "/src/index.ts": `export const x = 1;`,
+            "/src/App.vue": source,
+        });
+        let virtualFileAvailable = false;
+        using api = new API({
+            cwd: fileURLToPath(new URL("../../../../", import.meta.url).toString()),
+            fs: {
+                ...fs,
+                readFile: path => virtualFileAvailable && path === fileName ? source : fs.readFile!(path),
+                fileExists: path => virtualFileAvailable && path === fileName ? true : fs.fileExists!(path),
+            },
+        });
+        const snapshot = api.createSnapshot({
+            openProjects: ["/tsconfig.json"],
+            openFiles: ["/src/index.ts"],
+        });
+
+        const expectedError = /client error: failed to .*snapshot: no project found for opened file: \/src\/App\.vue\.ts/;
+        assert.throws(() => snapshot.update({ openFiles: [fileName] }), expectedError);
+        assert.throws(() => api.createSnapshot({ openFiles: [fileName] }), expectedError);
+
+        virtualFileAvailable = true;
+        const updated = snapshot.update({ openFiles: [fileName] });
+        const project = updated.getDefaultProjectForFile(fileName);
+        assert.ok(project);
+        assert.equal(project.configFileName, "");
+        assert.equal((project.program.getSourceFile(fileName))?.text, source);
+        assert.equal(snapshot.getDefaultProjectForFile(fileName), undefined);
+        assert.ok(updated.getConfiguredProject("/tsconfig.json"));
+
+        virtualFileAvailable = false;
+        const reopen = { openFiles: [fileName], fileNotifications: { deleted: [fileName] } };
+        assert.throws(() => updated.update(reopen), expectedError);
+        assert.equal((project.program.getSourceFile(fileName))?.text, source);
+    });
+
     test("finds inferred project for d.ts in node_modules after openFiles", () => {
         using api = spawnAPI({
             "/tsconfig.json": JSON.stringify({ compilerOptions: { strict: true } }),
diff --git a/tsc/internal/api/proto.go b/tsc/internal/api/proto.go
index e51b75fb9e8a3..6260b5eb77465 100644
--- a/tsc/internal/api/proto.go
+++ b/tsc/internal/api/proto.go
@@ -356,6 +356,7 @@ type SnapshotRequestChangesParams struct {
 	// tsconfig that contains it; if found, that configured project is loaded and
 	// becomes the file's default project. Otherwise the file is loaded into the
 	// inferred project (e.g. a node_modules d.ts not in any project's import graph).
+	// If a file cannot be loaded into any project, the request fails.
 	OpenFiles []DocumentIdentifier `json:"openFiles,omitempty"`
 	// CloseFiles lists files to release in the new snapshot. A file is only fully
 	// closed once every API client that opened it closes it.
diff --git a/tsc/internal/project/projectcollectionbuilder.go b/tsc/internal/project/projectcollectionbuilder.go
index 6264229c890f6..639c34c44bb9b 100644
--- a/tsc/internal/project/projectcollectionbuilder.go
+++ b/tsc/internal/project/projectcollectionbuilder.go
@@ -352,6 +352,9 @@ func (b *ProjectCollectionBuilder) HandleAPIRequest(apiRequest *APISnapshotReque
 	b.createdPrograms = createdPrograms
 	for uri := range apiRequest.EnsureFiles.Keys() {
 		b.DidRequestFile(uri, false /*configuredProjectsOnly*/, logger)
+		if b.findDefaultProject(uri.FileName(), b.toPath(uri.FileName())) == nil {
+			return fmt.Errorf("no project found for opened file: %s", uri.FileName())
+		}
 	}
 	for projectID := range apiRequest.EnsurePrograms.Keys() {
 		b.DidRequestProject(projectID, logger)