diff --git a/lib/github-package.js b/lib/github-package.js
index f0c88c6c99..99aa8fb59c 100644
--- a/lib/github-package.js
+++ b/lib/github-package.js
@@ -549,6 +549,29 @@ export default class GithubPackage {
    * projects and pane items.
    */
   async getNextContext(usePath = null) {
+    // Internal utility function to normalize paths not contained within a git
+    // working tree.
+    const workdirForNonGitPath = async sourcePath => {
+      const containingRoot = this.project.getDirectories().find(root => root.contains(sourcePath));
+      if (containingRoot) {
+        return containingRoot.getPath();
+      /* istanbul ignore else */
+      } else if (!(await fs.stat(sourcePath)).isDirectory()) {
+        return path.dirname(sourcePath);
+      } else {
+        return sourcePath;
+      }
+    };
+
+    // Internal utility function to identify the working directory to use for
+    // an arbitrary (file or directory) path.
+    const workdirForPath = async sourcePath => {
+      return (await Promise.all([
+        this.workdirCache.find(sourcePath),
+        workdirForNonGitPath(sourcePath),
+      ])).find(Boolean);
+    };
+
     // Identify paths that *could* contribute a git working directory to the pool. This is drawn from
     // the roots of open projects, the currently locked context if one is present, and the path of the
     // open workspace item.
@@ -574,7 +597,8 @@ export default class GithubPackage {
     const workdirs = new Set(
       await Promise.all(
         Array.from(candidatePaths, async candidatePath => {
-          const workdir = (await this.workdirCache.find(candidatePath)) || candidatePath;
+          const workdir = await workdirForPath(candidatePath);
+
           // Note the workdirs associated with the active pane item and the first open project so we can
           // prefer them later.
           if (candidatePath === activeItemPath) {
@@ -582,6 +606,7 @@ export default class GithubPackage {
           } else if (candidatePath === this.project.getPaths()[0]) {
             firstProjectWorkdir = workdir;
           }
+
           return workdir;
         }),
       ),
@@ -593,7 +618,17 @@ export default class GithubPackage {
     // 1 - Explicitly requested workdir. This is either selected by the user from a context tile or
     //     deserialized from package state. Choose this context only if it still exists in the pool.
     if (usePath) {
-      const stateContext = this.contextPool.getContext(usePath);
+      // Normalize usePath in a similar fashion to the way we do activeItemPath.
+      let useWorkdir = usePath;
+      if (usePath === activeItemPath) {
+        useWorkdir = activeItemWorkdir;
+      } else if (usePath === this.project.getPaths()[0]) {
+        useWorkdir = firstProjectWorkdir;
+      } else {
+        useWorkdir = await workdirForPath(usePath);
+      }
+
+      const stateContext = this.contextPool.getContext(useWorkdir);
       if (stateContext.isPresent()) {
         return stateContext;
       }
diff --git a/test/github-package.test.js b/test/github-package.test.js
index 67d50bcddd..dc1e07b410 100644
--- a/test/github-package.test.js
+++ b/test/github-package.test.js
@@ -455,6 +455,29 @@ describe('GithubPackage', function() {
           assert.strictEqual(githubPackage.getActiveWorkdir(), workdirPath2);
         });
 
+        it('uses a context associated with a project root for paths within that root', async function() {
+          const workdirPath4 = await getTempDir();
+          await fs.mkdir(path.join(workdirPath4, 'subdir'));
+          const itemPath4 = path.join(workdirPath4, 'subdir/file.txt');
+          await fs.writeFile(itemPath4, 'content\n');
+
+          await contextUpdateAfter(githubPackage, () => project.setPaths([workdirPath1, workdirPath4]));
+
+          assert.strictEqual(githubPackage.getActiveWorkdir(), workdirPath1);
+          await contextUpdateAfter(githubPackage, () => atomEnv.workspace.open(itemPath4));
+          assert.strictEqual(githubPackage.getActiveWorkdir(), workdirPath4);
+        });
+
+        it('uses a context of the containing directory for file item paths not in any root', async function() {
+          const workdirPath4 = await getTempDir();
+          const itemPath4 = path.join(workdirPath4, 'file.txt');
+          await fs.writeFile(itemPath4, 'content\n');
+
+          assert.strictEqual(githubPackage.getActiveWorkdir(), workdirPath1);
+          await contextUpdateAfter(githubPackage, () => atomEnv.workspace.open(itemPath4));
+          assert.strictEqual(githubPackage.getActiveWorkdir(), workdirPath4);
+        });
+
         it('does nothing if the context is locked', async function() {
           const itemPath2 = path.join(workdirPath2, 'c.txt');