diff --git a/cabal-install/cabal-install.cabal b/cabal-install/cabal-install.cabal
index 83628ab03d1..6340f46e89b 100644
--- a/cabal-install/cabal-install.cabal
+++ b/cabal-install/cabal-install.cabal
@@ -330,6 +330,7 @@ test-suite unit-tests
     other-modules:
       UnitTests.Distribution.Client.ArbitraryInstances
       UnitTests.Distribution.Client.BuildReport
+      UnitTests.Distribution.Client.CmdRun
       UnitTests.Distribution.Client.Configure
       UnitTests.Distribution.Client.FetchUtils
       UnitTests.Distribution.Client.Get
diff --git a/cabal-install/src/Distribution/Client/CmdRun.hs b/cabal-install/src/Distribution/Client/CmdRun.hs
index 237858f7b19..c49df39c3fe 100644
--- a/cabal-install/src/Distribution/Client/CmdRun.hs
+++ b/cabal-install/src/Distribution/Client/CmdRun.hs
@@ -13,6 +13,8 @@ module Distribution.Client.CmdRun
   , noExesProblem
   , selectPackageTargets
   , selectComponentTarget
+  , RunProblem (..)
+  , renderRunProblem
   ) where
 
 import Distribution.Client.Compat.Prelude hiding (toList)
@@ -78,6 +80,10 @@ import Distribution.Client.Utils
   , occursOnlyOrBefore
   )
 
+import Distribution.Package
+  ( packageName
+  )
+
 import Distribution.Simple.BuildToolDepends
   ( getAllInternalToolDependencies
   )
@@ -612,6 +618,7 @@ renderRunProblem (TargetProblemMatchesMultiple targetSelector targets) =
                 (map (componentNameRaw . availableTargetComponentName) . (`filterTargetsKind` targets) <$> [ExeKind, TestKind, BenchKind])
             )
       )
+    ++ renderRunProblemMatchesMultipleHint targets
 renderRunProblem (TargetProblemMultipleTargets selectorMap) =
   "The run command is for running a single executable at once. The targets "
     ++ renderListCommaAnd
@@ -646,3 +653,24 @@ renderRunProblem (TargetProblemNoExes targetSelector) =
     ++ " because "
     ++ plural (targetSelectorPluralPkgs targetSelector) "it does" "they do"
     ++ " not contain any executables."
+
+-- | Render a hint suggesting how to disambiguate which executable to run when
+-- a target matches multiple executable-like components.
+renderRunProblemMatchesMultipleHint :: [AvailableTarget ()] -> String
+renderRunProblemMatchesMultipleHint targets =
+  case exes of
+    [] -> ""
+    _ ->
+      "\nYou need to specify which executable cabal should use. Try one of those:\n"
+        ++ unlines
+          [ "- cabal run " ++ prettyShow pkgname ++ ":" ++ exe
+          | (pkgname, exe) <- exes
+          ]
+  where
+    exes =
+      sortNub
+        [ ( packageName (availableTargetPackageId target)
+          , componentNameRaw (availableTargetComponentName target)
+          )
+        | target <- filterTargetsKind ExeKind targets
+        ]
diff --git a/cabal-install/tests/UnitTests.hs b/cabal-install/tests/UnitTests.hs
index c38f65d40c1..4da370fe0af 100644
--- a/cabal-install/tests/UnitTests.hs
+++ b/cabal-install/tests/UnitTests.hs
@@ -3,6 +3,7 @@ module Main (main) where
 import Test.Tasty
 
 import qualified UnitTests.Distribution.Client.BuildReport
+import qualified UnitTests.Distribution.Client.CmdRun
 import qualified UnitTests.Distribution.Client.Configure
 import qualified UnitTests.Distribution.Client.FetchUtils
 import qualified UnitTests.Distribution.Client.GZipUtils
@@ -36,6 +37,9 @@ main = do
       [ testGroup
           "UnitTests.Distribution.Client.BuildReport"
           UnitTests.Distribution.Client.BuildReport.tests
+      , testGroup
+          "UnitTests.Distribution.Client.CmdRun"
+          UnitTests.Distribution.Client.CmdRun.tests
       , testGroup
           "UnitTests.Distribution.Client.Configure"
           UnitTests.Distribution.Client.Configure.tests
diff --git a/cabal-install/tests/UnitTests/Distribution/Client/CmdRun.hs b/cabal-install/tests/UnitTests/Distribution/Client/CmdRun.hs
new file mode 100644
index 00000000000..bbaf9012141
--- /dev/null
+++ b/cabal-install/tests/UnitTests/Distribution/Client/CmdRun.hs
@@ -0,0 +1,109 @@
+module UnitTests.Distribution.Client.CmdRun
+  ( tests
+  ) where
+
+import Distribution.Client.CmdRun
+  ( RunProblem (..)
+  , renderRunProblem
+  )
+import Distribution.Client.ProjectPlanning
+  ( AvailableTarget (..)
+  , AvailableTargetStatus (..)
+  , TargetRequested (..)
+  )
+import Distribution.Client.TargetSelector
+  ( TargetSelector (..)
+  )
+
+import Distribution.Package (PackageIdentifier (..), PackageName, mkPackageName)
+import Distribution.Types.ComponentName (ComponentName (..))
+import Distribution.Types.UnqualComponentName (mkUnqualComponentName)
+import Distribution.Version (mkVersion)
+
+import Data.List (isInfixOf)
+
+import Test.Tasty
+import Test.Tasty.HUnit
+
+tests :: [TestTree]
+tests =
+  [ testCase "hints at each executable when there are multiple" testMultipleExecutablesHint
+  , testCase "hint lists only executables" testHintListsOnlyExecutables
+  , testCase "no hint when there are no executables" testNoHintWithoutExecutables
+  ]
+
+pkgname :: PackageName
+pkgname = mkPackageName "agent-cli"
+
+pkgid :: PackageIdentifier
+pkgid = PackageIdentifier pkgname (mkVersion [0, 1, 0, 0])
+
+mkTarget :: ComponentName -> AvailableTarget ()
+mkTarget cname =
+  AvailableTarget
+    { availableTargetPackageId = pkgid
+    , availableTargetComponentName = cname
+    , availableTargetStatus = TargetBuildable () TargetRequestedByDefault
+    , availableTargetLocalToProject = True
+    }
+
+exe :: String -> AvailableTarget ()
+exe = mkTarget . CExeName . mkUnqualComponentName
+
+test :: String -> AvailableTarget ()
+test = mkTarget . CTestName . mkUnqualComponentName
+
+bench :: String -> AvailableTarget ()
+bench = mkTarget . CBenchName . mkUnqualComponentName
+
+selector :: TargetSelector
+selector = TargetPackageNamed pkgname Nothing
+
+testMultipleExecutablesHint :: Assertion
+testMultipleExecutablesHint = do
+  let rendered =
+        renderRunProblem $
+          TargetProblemMatchesMultiple
+            selector
+            [ exe "agent-cli"
+            , exe "agent-telegram"
+            , exe "eval-ghci-vs-bash"
+            ]
+  assertBool "hint header is present" $
+    "You need to specify which executable cabal should use. Try one of those:"
+      `isInfixOf` rendered
+  mapM_ (assertSuggestion rendered) ["agent-cli", "agent-telegram", "eval-ghci-vs-bash"]
+
+testHintListsOnlyExecutables :: Assertion
+testHintListsOnlyExecutables = do
+  let rendered =
+        renderRunProblem $
+          TargetProblemMatchesMultiple
+            selector
+            [ exe "agent-cli"
+            , exe "agent-telegram"
+            , test "agent-cli-test"
+            , bench "image-preview-latency-bench"
+            ]
+  assertBool "test suite is not suggested" $
+    not ("- cabal run agent-cli:agent-cli-test" `isInfixOf` rendered)
+  assertBool "benchmark is not suggested" $
+    not ("- cabal run agent-cli:image-preview-latency-bench" `isInfixOf` rendered)
+  mapM_ (assertSuggestion rendered) ["agent-cli", "agent-telegram"]
+
+testNoHintWithoutExecutables :: Assertion
+testNoHintWithoutExecutables = do
+  let rendered =
+        renderRunProblem $
+          TargetProblemMatchesMultiple
+            selector
+            [ test "agent-cli-test"
+            , bench "image-preview-latency-bench"
+            ]
+  assertBool "no hint when there are no executables" $
+    not ("You need to specify which executable" `isInfixOf` rendered)
+
+assertSuggestion :: String -> String -> Assertion
+assertSuggestion rendered exeName =
+  assertBool ("suggestion for executable " ++ exeName) $
+    ("- cabal run agent-cli:" ++ exeName) `isInfixOf` rendered
diff --git a/cabal-testsuite/PackageTests/NewBuild/CmdRun/MultipleExes/cabal.out b/cabal-testsuite/PackageTests/NewBuild/CmdRun/MultipleExes/cabal.out
index 2223a88a94c..ed4e8212c04 100644
--- a/cabal-testsuite/PackageTests/NewBuild/CmdRun/MultipleExes/cabal.out
+++ b/cabal-testsuite/PackageTests/NewBuild/CmdRun/MultipleExes/cabal.out
@@ -19,8 +19,16 @@ Error: [Cabal-7070]
 The run command is for running a single executable at once. The target '' refers to the package MultipleExes-1.0 which includes 
 - executables: bar and foo
 
+You need to specify which executable cabal should use. Try one of those:
+- cabal run MultipleExes:bar
+- cabal run MultipleExes:foo
+
 # cabal v2-run
 Error: [Cabal-7070]
 The run command is for running a single executable at once. The target 'MultipleExes' refers to the package MultipleExes-1.0 which includes 
 - executables: bar and foo
 
+You need to specify which executable cabal should use. Try one of those:
+- cabal run MultipleExes:bar
+- cabal run MultipleExes:foo
+
diff --git a/cabal-testsuite/PackageTests/NewBuild/CmdRun/MultiplePackages/cabal.out b/cabal-testsuite/PackageTests/NewBuild/CmdRun/MultiplePackages/cabal.out
index 7f851dca6a8..e4002869612 100644
--- a/cabal-testsuite/PackageTests/NewBuild/CmdRun/MultiplePackages/cabal.out
+++ b/cabal-testsuite/PackageTests/NewBuild/CmdRun/MultiplePackages/cabal.out
@@ -29,6 +29,10 @@ Error: [Cabal-7070]
 The run command is for running a single executable at once. The target 'bar' refers to the package bar-1.0 which includes 
 - executables: bar-exe and foo-exe
 
+You need to specify which executable cabal should use. Try one of those:
+- cabal run bar:bar-exe
+- cabal run bar:foo-exe
+
 # cabal v2-run
 Error: [Cabal-7132]
 Ambiguous target 'foo-exe'. It could be:
diff --git a/changelog.d/12266.md b/changelog.d/12266.md
new file mode 100644
index 00000000000..2568f45b82e
--- /dev/null
+++ b/changelog.d/12266.md
@@ -0,0 +1,25 @@
+---
+synopsis: Suggest a concrete target when `cabal run` matches multiple executables
+packages: [cabal-install]
+prs: 12266
+issues: 12262
+---
+
+The `cabal run` command previously failed with an error that listed the
+components of a package but did not explain how to pick one:
+
+```diff
+  Error: [Cabal-7070]
+  The run command is for running a single executable at once. The target 'agent-cli' refers to the package agent-cli-0.1.0.0 which includes
+  - executables: agent-cli, agent-telegram and eval-ghci-vs-bash
+  - test-suites: agent-cli-test
+  - benchmarks: image-preview-latency-bench and subagent-retention-bench
++
++ You need to specify which executable cabal should use. Try one of those:
++ - cabal run agent-cli:agent-cli
++ - cabal run agent-cli:agent-telegram
++ - cabal run agent-cli:eval-ghci-vs-bash
+```
+
+The hint lists the executables of the target package and is only shown when
+there is more than one executable to choose from.