diff --git a/__tests__/utils.test.ts b/__tests__/utils.test.ts
index f5e364788..122c75347 100644
--- a/__tests__/utils.test.ts
+++ b/__tests__/utils.test.ts
@@ -10,7 +10,7 @@ import {
   validatePythonVersionFormatForPyPy,
   isCacheFeatureAvailable,
   getVersionInputFromFile,
-  getVersionInputFromPlainFile,
+  getVersionsInputFromPlainFile,
   getVersionInputFromTomlFile,
   getNextPageUrl
 } from '../src/utils';
@@ -91,7 +91,7 @@ const tempDir = path.join(
 );
 
 describe('Version from file test', () => {
-  it.each([getVersionInputFromPlainFile, getVersionInputFromFile])(
+  it.each([getVersionsInputFromPlainFile, getVersionInputFromFile])(
     'Version from plain file test',
     async _fn => {
       await io.mkdirP(tempDir);
@@ -102,6 +102,28 @@ describe('Version from file test', () => {
       expect(_fn(pythonVersionFilePath)).toEqual([pythonVersionFileContent]);
     }
   );
+  it.each([getVersionsInputFromPlainFile, getVersionInputFromFile])(
+    'Versions from multiline plain file test',
+    async _fn => {
+      await io.mkdirP(tempDir);
+      const pythonVersionFileName = 'python-version.file';
+      const pythonVersionFilePath = path.join(tempDir, pythonVersionFileName);
+      const pythonVersionFileContent = '3.8\r\n3.7';
+      fs.writeFileSync(pythonVersionFilePath, pythonVersionFileContent);
+      expect(_fn(pythonVersionFilePath)).toEqual(['3.8', '3.7']);
+    }
+  );
+  it.each([getVersionsInputFromPlainFile, getVersionInputFromFile])(
+    'Version from complex plain file test',
+    async _fn => {
+      await io.mkdirP(tempDir);
+      const pythonVersionFileName = 'python-version.file';
+      const pythonVersionFilePath = path.join(tempDir, pythonVersionFileName);
+      const pythonVersionFileContent = '3.10/envs/virtualenv\r# 3.9\n3.8\r\n3.7\r\n 3.6 \r\n';
+      fs.writeFileSync(pythonVersionFilePath, pythonVersionFileContent);
+      expect(_fn(pythonVersionFilePath)).toEqual(['3.10', '3.8', '3.7', '3.6']);
+    }
+  );
   it.each([getVersionInputFromTomlFile, getVersionInputFromFile])(
     'Version from standard pyproject.toml test',
     async _fn => {
diff --git a/src/setup-python.ts b/src/setup-python.ts
index 0dd45f0ca..329fe9e71 100644
--- a/src/setup-python.ts
+++ b/src/setup-python.ts
@@ -11,7 +11,7 @@ import {
   logWarning,
   IS_MAC,
   getVersionInputFromFile,
-  getVersionInputFromPlainFile
+  getVersionsInputFromPlainFile
 } from './utils';
 
 function isPyPyVersion(versionSpec: string) {
@@ -35,7 +35,7 @@ async function cacheDependencies(cache: string, pythonVersion: string) {
 
 function resolveVersionInputFromDefaultFile(): string[] {
   const couples: [string, (versionFile: string) => string[]][] = [
-    ['.python-version', getVersionInputFromPlainFile]
+    ['.python-version', getVersionsInputFromPlainFile]
   ];
   for (const [versionFile, _fn] of couples) {
     logWarning(
diff --git a/src/utils.ts b/src/utils.ts
index 644b4af5f..1ec455075 100644
--- a/src/utils.ts
+++ b/src/utils.ts
@@ -222,7 +222,7 @@ function extractValue(obj: any, keys: string[]): string | undefined {
  * If none is present, returns an empty list.
  */
 export function getVersionInputFromTomlFile(versionFile: string): string[] {
-  core.debug(`Trying to resolve version form ${versionFile}`);
+  core.debug(`Trying to resolve version from ${versionFile}`);
 
   const pyprojectFile = fs.readFileSync(versionFile, 'utf8');
   const pyprojectConfig = toml.parse(pyprojectFile);
@@ -260,13 +260,28 @@ export function getVersionInputFromTomlFile(versionFile: string): string[] {
 }
 
 /**
- * Python version extracted from a plain text file.
+ * Python versions extracted from a plain text file.
+ * - Resolves multiple versions from multiple lines.
+ * - Handles pyenv-virtualenv pointers (e.g. `3.10/envs/virtualenv`).
+ * - Ignores empty lines and lines starting with `#`
+ * - Trims whitespace.
  */
-export function getVersionInputFromPlainFile(versionFile: string): string[] {
-  core.debug(`Trying to resolve version form ${versionFile}`);
-  const version = fs.readFileSync(versionFile, 'utf8').trim();
-  core.info(`Resolved ${versionFile} as ${version}`);
-  return [version];
+export function getVersionsInputFromPlainFile(versionFile: string): string[] {
+  core.debug(`Trying to resolve versions from ${versionFile}`);
+  const content = fs.readFileSync(versionFile, 'utf8').trim();
+  const lines = content.split(/\r\n|\r|\n/);
+  const versions = lines
+    .map(line => {
+      if (line.startsWith('#') || line.trim() === '') {
+        return undefined;
+      }
+      let version: string = line.trim();
+      version = version.split('/')[0];
+      return version;
+    })
+    .filter(version => version !== undefined) as string[];
+  core.info(`Resolved ${versionFile} as ${versions.join(', ')}`);
+  return versions;
 }
 
 /**
@@ -276,7 +291,7 @@ export function getVersionInputFromFile(versionFile: string): string[] {
   if (versionFile.endsWith('.toml')) {
     return getVersionInputFromTomlFile(versionFile);
   } else {
-    return getVersionInputFromPlainFile(versionFile);
+    return getVersionsInputFromPlainFile(versionFile);
   }
 }