diff --git a/tools/catalog.js b/tools/catalog.js
index 2c71d012e2..f15a7e9874 100644
--- a/tools/catalog.js
+++ b/tools/catalog.js
@@ -205,10 +205,12 @@ _.extend(Catalog.prototype, {
      });
     }
 
+    var project = require("./project.js").project;
     // If we are called with 'ignore projectDeps', then we don't even look to
     // see what the project thinks is the reasonable version answer. We
-    // recalculate everything.
-    if (opts.ignoreProjectDeps) {
+    // recalculate everything. Also, if the project root path has not been
+    // initialized, we probably can't use the project's dependencies.
+    if (opts.ignoreProjectDeps || !project.rootDir) {
       return self.resolver.resolve(deps, constr, resolverOpts);
     }
 
@@ -222,7 +224,6 @@ _.extend(Catalog.prototype, {
     // We do this, because when we record the local version lock files, we don't
     // want to record irrelevant dependencies (since we don't want those files
     // changing randomly).
-    var project = require("./project.js").project;
     var versions = project.getVersions();
     resolverOpts.previousSolution = versions;
     var solution = self.resolver.resolve(deps, constr, resolverOpts);
diff --git a/tools/project.js b/tools/project.js
index 7e9a921b98..6c174aa20e 100644
--- a/tools/project.js
+++ b/tools/project.js
@@ -81,7 +81,8 @@ var Project = function () {
 
   // Packages & versions of all dependencies, including transitive dependencies,
   // program dependencies and so on, that this project uses. An object mapping a
-  // package name to its string version. Derived from self.combinedConstraints.
+  // package name to its string version. Derived from self.combinedConstraints
+  // and recorded in the .meteor/versions file.
   self.dependencies = null;
 
   // The package loader for this project, with the project's dependencies as its
@@ -93,13 +94,11 @@ var Project = function () {
   // by any constraint-related operations.
   self.appId = null;
 
-  // True if the project has been initialized with a root directory and
-  // dependency information and false otherwise.
-  self.initialized = false;
-
-  // Packages used by the sub-programs using of this project. Should not change
-  // without restart, we memoize this because we would otherwise need to reread
-  // it from disk every time we recalculate versions.
+  // Packages used by the sub-programs using of this project. Will not change
+  // while the app is running! Therefore, we can remember it, so we don't need
+  // to perform a bunch of reads when we recalculate combinedConstraints.
+  //
+  // XXX: Is this actually faster?
   self._programConstraints = null;
 
   // Whenever we change the constraints, we invalidate many constraint-related
@@ -171,6 +170,17 @@ _.extend(Project.prototype, {
     self._depsUpToDate = false;
   },
 
+  // Rereads all the on-disk files by reinitalizing the project with the same directory.
+  //
+  // We don't automatically reinitialize this singleton when an app is
+  // restarted, but an app restart is very likely caused by changes to our
+  // package configuration files. So, make sure to reload the constraints &
+  // dependencies here.
+  reload : function () {
+    var self = this;
+    self.setRootDir(self.rootDir);
+  },
+
   // Several fields in project are derived from constraints. Whenever we change
   // the constraints, we invalidate those fields, when we call on
   // dependency-related operations, we recompute them as needed.
@@ -181,20 +191,22 @@ _.extend(Project.prototype, {
   _ensureDepsUpToDate : function () {
     var self = this;
 
-    // Aha, now we can initialize the project singleton. There is a dependency
-    // chain here -- to calculate project dependencies, we need to know what
-    // release we are on. So, we need to initialize it after the release. To
-    // figure out our release, we need to initialize the catalog. But we can't use
-    // the catalog's constraint solver until we initialize the release.
-    //
-    // Because this call is lazy, we don't need to worry about this, as long as we
-    // call things in the right order in main.js
+    // To calculate project dependencies, we need to know what release we are
+    // on, but to do that, we need to have a rootDirectory. So, we initialize
+    // the path first, and call 'ensureDepsUpToDate' lazily.
     if (!release.current) {
       throw new Error(
         "need to compute release before computing project dependencies.");
     }
 
     if (!self._depsUpToDate) {
+
+      // XXX: I don't understand why we don't reread this automatically.
+      self.constraints = processPerConstraintLines(
+        getLines(self._constraintFile));
+      self.dependencies = processPerConstraintLines(
+         getLines(self._versionsFile));
+
       // Use current release to calculate packages & combined constraints.
       var releasePackages = release.current.isProperRelease() ?
             release.current.getPackages() : {};
@@ -343,8 +355,6 @@ _.extend(Project.prototype, {
     return path.join(self.rootDir, '.meteor', 'packages');
   },
 
-
-
   // Give the contents of the project's .meteor/versions file to the caller.
   //
   // Returns an object mapping package name to its string version.
diff --git a/tools/run-app.js b/tools/run-app.js
index b758606098..3e51e9459e 100644
--- a/tools/run-app.js
+++ b/tools/run-app.js
@@ -389,6 +389,7 @@ _.extend(AppRunner.prototype, {
   _runOnce: function (onListen) {
     var self = this;
 
+    project.reload();
     runLog.clearLog();
     self.proxy.setMode("hold");
 
diff --git a/tools/tests/add-package.js b/tools/tests/add-package.js
index 9658272431..673061280a 100644
--- a/tools/tests/add-package.js
+++ b/tools/tests/add-package.js
@@ -108,7 +108,6 @@ selftest.define("change packages", function () {
   run.waitSecs(5);
   run.match("running at");
   run.match("localhost");
-
   // Add the local package 'say-something'. It should print a message.
   s.write(".meteor/packages", "standard-app-packages \n say-something");
   run.waitSecs(2);
@@ -144,7 +143,6 @@ selftest.define("change packages", function () {
 
   run.waitSecs(2);
   run.match("restarted");
-
 });
 
 
@@ -161,6 +159,7 @@ selftest.define("add packages", function () {
 
   console.log("XXX: this assumes that we are running from checkout");
   run = s.run("add", "accounts-base", "--offline-catalog");
+
   run.match("Successfully added");
   checkPackages(s,
                 ["accounts-base", "standard-app-packages"]);
@@ -168,7 +167,9 @@ selftest.define("add packages", function () {
   run = s.run("--once");
 
   run = s.run("add", "say-something@1.0.0", "--offline-catalog");
+
   run.match("Successfully added");
+
   checkPackages(s,
                 ["accounts-base",  "say-something@1.0.0", "standard-app-packages"]);
 
@@ -184,16 +185,15 @@ selftest.define("add packages", function () {
                  "contains-plugin@1.1.0+local"]);
 
   run = s.run("remove", "say-something", "--offline-catalog");
-  run.match("Removed say-something");
+  run.match("Removed constraint say-something");
   checkVersions(s,
                 ["accounts-base",  "depends-on-plugin",
                  "standard-app-packages",
                  "contains-plugin"]);
 
-
   run = s.run("remove", "depends-on-plugin", "--offline-catalog");
   run.match("removed dependency on contains-plugin");
-  run.match("Removed depends-on-plugin");
+  run.match("Removed constraint depends-on-plugin");
 
   checkVersions(s,
                 ["accounts-base",